Biology subjects

Patel, N. H.

Publications and source records attributed to Patel, N. H..

11 recordsLinked to original sources

bioRxiv2024

Lepidopteran scale cells derive from sensory organ precursors through a canonical lineage

The success of butterflies and moths is tightly linked to the origin of scales within the group. A long-standing hypothesis postulates that scales are homologous to the well-described mechanosensory bristles found in the fruit fly Drosophila melanogaster, where both derive from an epithelial precursor specified by lateral inhibition that then undergoes multiple rounds of division. Previous histological examination and candidate gene approaches identified parallels in genes involved in scale and bristle development. Here, we provide definitive developmental and transcriptomic evidence that the differentiation of lepidopteran scales derives from the canonical cell lineage, known as the Sensory Organ Precursor (SOP). Live imaging in moth and butterfly pupae shows that SOP cells undergo two rounds of asymmetric divisions that first abrogate the neurogenic lineage, and then lead to a differentiated scale precursor and its associated socket cell. Single-nucleus RNA sequencing across a time-series of early pupal development revealed differential gene expression patterns that mirror canonical lineage development, including Notch-Delta signalling components, cell adhesion molecules, cell cycling factors, and terminal cell differentiation markers, suggesting a shared origin of the SOP developmental program. Additionally, we recovered a novel gene, the POU-domain transcription factor pdm3, involved in the proper differentiation of butterfly wing scales. Altogether, these data open up avenues for understanding scale type specification and development, and illustrate how single-cell transcriptomics provide a powerful platform for understanding the evolution of cell types.

developmental biology↗

bioRxiv2024

A novel expression domain of extradenticle underlies the evolutionary developmental origin of the chelicerate patella

Neofunctionalization of duplicated gene copies is thought to be an important process underlying the origin of evolutionary novelty and provides an elegant mechanism for the origin of new phenotypic traits. One putative case where a new gene copy has been linked to a novel morphological trait is the origin of the arachnid patella, a taxonomically restricted leg segment. In spiders, the origin of this segment has been linked to the origin of the paralog dachshund-2, suggesting that a new gene facilitated the expression of a new trait. However, various arachnid groups that possess patellae do not have a copy of dachshund-2, disfavoring the direct link between gene origin and trait origin. We investigated the developmental genetic basis for patellar patterning in the harvestman Phalangium opilio, which lacks dachshund-2. Here, we show that the harvestman patella is established by a novel expression domain of the transcription factor extradenticle. Leveraging this definition of patellar identity, we surveyed targeted groups across chelicerate phylogeny to assess when this trait evolved. We show that a patellar homolog is present in Pycnogonida (sea spiders) and various arachnid orders, suggesting a single origin of the patella in the ancestor of Chelicerata. A potential loss of the patella is observed in Ixodida. Our results suggest that the modification of an ancient gene, rather than the neofunctionalization of a new gene copy, underlies the origin of the patella. Broadly, this work underscores the value of comparative data and broad taxonomic sampling when testing hypotheses in evolutionary developmental biology.

evolutionary biology↗

bioRxiv2022

Distinct regulation of Hox genes by Polycomb Group genes in a crustacean

Non-insect crustaceans exhibit tremendous body plan diversity. The evolution of diverse patterns of Hox gene expression has been implicated as a primary driver of body plan evolution between crustacean groups, but the mechanisms underlying Hox regulatory evolution remain unknown. We identify Polycomb and Trithorax Group proteins, crucial for proper Hox regulation across bilaterians, in the genome of the amphipod crustacean Parhyale hawaiensis, and demonstrate their essential functions in crustacean Hox regulation and embryonic development using CRISPR-Cas9 mutagenesis. Examination of Hox misexpression patterns between individual Hox genes with respect to timing, tissue, and PcG mutant gene in mutant embryos reveals that each crustacean Hox gene follows its own idiosyncratic regulatory mechanism. These results suggest a distinct regulation of Hox genes that may have enabled crustacean body plan evolution. Primary Findings- The genome of the amphipod crustacean Parhyale hawaiensis contains all core Polycomb Group (PcG) and Trithorax Group (TrxG) proteins - CRISPR-Cas9 mutagenesis of PcG proteins induces homeotic transformations and misexpression of Hox genes that differ from similar experiments in insects - PcG knockout embryos show proper initiation of Hox expression boundaries at early developmental stages - Each of the three posterior Hox genes in Parhyale displays distinct patterns of misexpression in response to PcG knockout - Hox regulation appears to occur via different mechanisms in the nervous system vs. limbs - PcG phenotypes reveal the potential for distinct layers of Hox regulation in crustaceans O_FIG O_LINKSMALLFIG WIDTH=193 HEIGHT=200 SRC="FIGDIR/small/485719v1_ufig1.gif" ALT="Figure 1"> View larger version (59K): org.highwire.dtl.DTLVardef@7508a7org.highwire.dtl.DTLVardef@18b0c2dorg.highwire.dtl.DTLVardef@1cc602corg.highwire.dtl.DTLVardef@bdf7fc_HPS_FORMAT_FIGEXP M_FIG C_FIG

developmental biology↗

bioRxiv2022

Combinatorial interactions of Hox genes establish appendage diversity of the amphipod crustacean Parhyale hawaiensis

Hox genes establish regional identity along the anterior-posterior axis in diverse animals. Changes in Hox expression can induce striking homeotic transformations, where one region of the body is transformed into another. Previous work in Drosophila has demonstrated that Hox cross-regulatory interactions are crucial for maintaining proper Hox expression. One major mechanism is the phenomenon of "posterior prevalence", wherein anterior Hox genes are repressed by more posterior Hox genes. Loss of posterior Hox expression under this model would predict posterior-to-anterior transformations, as is frequently observed in Drosophila. While posterior prevalence is thought to occur in many animals, studies of such Hox cross-regulation have focused on a limited number of organisms. In this paper, we examine the cross-regulatory interactions of three Hox genes, Ultrabithorax (Ubx), abdominal-A (abd-A), and Abdominal-B (Abd-B) in patterning thoracic and abdominal appendages in the amphipod crustacean Parhyale hawaiensis. Studies of Hox function in Parhyale have previously revealed two striking phenotypes which differed markedly from what a "posterior prevalence" model would predict, including non-contiguous and anterior-to-posterior transformations. We probe the logic of Parhyale Hox cross-regulation by using CRISPR/Cas9 to systematically examine all combinations of Ubx, abd-A, and Abd-B loss of function in Parhyale. By analyzing homeotic phenotypes and examining the expression of additional Hox genes, we reveal Hox cross-regulatory interactions in Parhyale. From these data, we also demonstrate that some Parhyale Hox genes function combinatorially to specify posterior limb identity, rather than abiding by a posterior prevalence mechanism. These results provide evidence that combinatorial Hox interactions may be responsible for the tremendous body plan diversity of crustaceans. Graphical Abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=192 SRC="FIGDIR/small/485717v1_ufig1.gif" ALT="Figure 1"> View larger version (43K): org.highwire.dtl.DTLVardef@16bfc85org.highwire.dtl.DTLVardef@8f859eorg.highwire.dtl.DTLVardef@8d7892org.highwire.dtl.DTLVardef@1e6c9f0_HPS_FORMAT_FIGEXP M_FIG C_FIG

developmental biology↗

bioRxiv2021

The Daphnia carapace and the origin of novel structures

Understanding how novel structures arise is a central question in evolution. Novel structures are often defined as structures that are not derived from (homologous to) any structure in the ancestor1. The carapace of the water flea Daphnia magna is a bivalved "cape" of exoskeleton that has been proposed to be one of many novel arthropod structures that arose through repeated co-option of genes that also pattern insect wings2-4. To determine whether the Daphnia carapace is a novel structure, we compare the expression of pannier, araucan, and vestigial between Daphnia, Parhyale, and Tribolium. Our results suggest that the Daphnia carapace did not arise by co-option, but instead derives from an exite (lateral lobe) that emerges from an ancestral proximal leg segment that was incorporated into the Daphnia body wall. The Daphnia carapace therefore appears to be homologous to the Parhyale tergal plate and the insect wing5. Remarkably, the vestigial-positive region that gives rise to the Daphnia carapace appears to be present in Parhyale6 and Tribolium as a small, inconspicuous protrusion. Similarly, the vestigial-positive regions that form thoracic tergal plates in Parhyale appear to be present in Daphnia, even though Daphnia does not form thoracic tergal plates. Thus, rather than a novel structure resulting from gene co-option, the Daphnia carapace appears to have arisen from a shared, ancestral tissue (morphogenetic field) that persists in a cryptic state in other arthropod lineages. Cryptic persistence of unrecognized serial homologs may thus be a general solution for the origin of novel structures.

developmental biology↗

bioRxiv2021

Identification and classification of cis-regulatory elements in the amphipod crustacean Parhyale hawaiensis

Emerging research organisms enable the study of biology that cannot be addressed using classical "model" organisms. The development of new data resources can accelerate research in such animals. Here, we present new functional genomic resources for the amphipod crustacean Parhyale hawaiensis, facilitating the exploration of gene regulatory evolution using this emerging research organism. We use Omni-ATAC-Seq, an improved form of the Assay for Transposase-Accessible Chromatin coupled with next-generation sequencing (ATAC-Seq), to identify accessible chromatin genome-wide across a broad time course of Parhyale embryonic development. This time course encompasses many major morphological events, including segmentation, body regionalization, gut morphogenesis, and limb development. In addition, we use short- and long-read RNA-Seq to generate an improved Parhyale genome annotation, enabling deeper classification of identified regulatory elements. We discover differential accessibility, predict nucleosome positioning, infer transcription factor binding, cluster peaks based on accessibility dynamics, classify biological functions, and correlate gene expression with accessibility. Using a Minos transposase reporter system, we demonstrate the potential to identify novel regulatory elements using this approach, including distal regulatory elements. This work provides a platform for the identification of novel developmental regulatory elements in Parhyale, and offers a framework for performing such experiments in other emerging research organisms. Primary Findings- Omni-ATAC-Seq identifies cis-regulatory elements genome-wide during crustacean embryogenesis - Combined short- and long-read RNA-Seq improves the Parhyale genome annotation - ImpulseDE2 analysis identifies dynamically regulated candidate regulatory elements - NucleoATAC and HINT-ATAC enable inference of nucleosome occupancy and transcription factor binding - Fuzzy clustering reveals peaks with distinct accessibility and chromatin dynamics - Integration of accessibility and gene expression reveals possible enhancers and repressors - Omni-ATAC can identify known and novel regulatory elements O_FIG O_LINKSMALLFIG WIDTH=196 HEIGHT=200 SRC="FIGDIR/small/460328v2_ufig1.gif" ALT="Figure 1"> View larger version (49K): org.highwire.dtl.DTLVardef@1f849b6org.highwire.dtl.DTLVardef@1af655borg.highwire.dtl.DTLVardef@274baaorg.highwire.dtl.DTLVardef@1d8af02_HPS_FORMAT_FIGEXP M_FIG C_FIG

developmental biology↗

bioRxiv2020

Convergence in light transmission properties of transparent wing areas in clearwing mimetic butterflies

Mullerian mimicry is a positive interspecific interaction, whereby co-occurring defended prey species share a common aposematic signal. In Lepidoptera, aposematic species typically harbour conspicuous opaque wing colour patterns with convergent optical properties among co-mimetic species. Surprisingly, some aposematic mimetic species have partially transparent wings, raising the questions of whether optical properties of transparent patches are also convergent, and of how transparency is achieved. Here we conducted a comparative study of wing optics, micro and nanostructures in neotropical mimetic clearwing Lepidoptera, using spectrophotometry and microscopy imaging. We show that transparency, as perceived by predators, is convergent among co-mimics. Underlying micro- and nanostructures are also convergent despite a large structural diversity. We reveal that while transparency is primarily produced by microstructure modifications, nanostructures largely influence light transmission, maybe enabling additional fine-tuning in transmission properties. This study shows that transparency might not only enable camouflage but can also be part of aposematic signals.

evolutionary biology↗

bioRxiv2020

Developmental, cellular, and biochemical basis of transparency in the glasswing butterfly Greta oto

Numerous species of Lepidoptera have transparent wings, which often possess scales of altered morphology and reduced size, and the presence of membrane surface nanostructures that dramatically reduce reflection. Optical properties and anti-reflective nanostructures have been characterized for several clearwing Lepidoptera, but the developmental basis of wing transparency is unknown. We apply confocal and electron microscopy to create a developmental time-series in the glasswing butterfly, Greta oto, comparing transparent and non-transparent wing regions. We find that scale precursor cell density is reduced in transparent regions, and cytoskeletal organization differs between flat scales in opaque regions, and thin, bristle-like scales in transparent regions. We also reveal that sub-wavelength nanopillars on the wing membrane are wax-based, derive from wing epithelial cells and their associated microvillar projections, and demonstrate their role in enhancing-anti-reflective properties. These findings provide insight into morphogenesis of naturally organized micro- and nanostructures and may provide bioinspiration for new anti-reflective materials.

developmental biology↗

bioRxiv2019

Structural color in Junonia butterflies evolves by tuning scale lamina thickness

In diverse organisms, nanostructures that coherently scatter light create structural color, but how such structures are built remains mysterious. We investigate the evolution and genetic regulation of butterfly scale laminae, which are simple photonic nanostructures. In a lineage of buckeye butterflies artificially selected for blue wing color, we found that thickened laminae caused a color shift from brown to blue. Deletion of the optix wing patterning gene also altered color via lamina thickening, revealing shared genetic regulation of pigments and lamina thickness. Finally, we show how lamina thickness variation contributes to the color diversity that distinguishes sexes and species throughout the genus Junonia. Thus, quantitatively tuning one dimension of scale architecture facilitates both the microevolution and macroevolution of a broad spectrum of hues. Because the lamina is an intrinsic component of typical butterfly scales, our findings suggest that tuning lamina thickness is a readily accessible mechanism to create structural color across the Lepidoptera.

evolutionary biology↗

bioRxiv2018

Nanopore sequencing of long ribosomal DNA amplicons enables portable and simple biodiversity assessments with high phylogenetic resolution across broad taxonomic scale

BackgroundIn light of the current biodiversity crisis, DNA barcoding is developing into an essential tool to quantify state shifts in global ecosystems. Current barcoding protocols often rely on short amplicon sequences, which yield accurate identification of biological entities in a community, but provide limited phylogenetic resolution across broad taxonomic scales. However, the phylogenetic structure of communities is an essential component of biodiversity. Consequently, a barcoding approach is required that unites robust taxonomic assignment power and high phylogenetic utility. A possible solution is offered by sequencing long ribosomal DNA (rDNA) amplicons on the MinION platform (Oxford Nanopore Technologies).\n\nResultsUsing a dataset of various animal and plant species, with a focus on arthropods, we assemble a pipeline for long rDNA barcode analysis and introduce a new software (MiniBar) to demultiplex dual indexed nanopore reads. We find excellent phylogenetic and taxonomic resolution offered by long rDNA sequences across broad taxonomic scales. We highlight the simplicity of our approach by field barcoding with a miniaturized, mobile laboratory in a remote rainforest. We also test the utility of long rDNA amplicons for analysis of community diversity through metabarcoding and find that they recover highly skewed diversity estimates.\n\nConclusionsSequencing dual indexed, long rDNA amplicons on the MinION platform is a straightforward, cost effective, portable and universal approach for eukaryote DNA barcoding. Long rDNA amplicons scale up DNA barcoding by enabling the accurate recovery of taxonomic and phylogenetic diversity. However, bulk community analyses using long-read approaches may introduce biases and will require further exploration.

ecology↗

bioRxiv2018

Insect wings and body wall evolved from ancient leg segments

The origin of insect wings has long been debated. Central to this debate is whether wings evolved from an epipod (outgrowth, e.g., a gill) on ancestral crustacean leg segments, or represent a novel outgrowth from the dorsal body wall that co-opted some of the genes used to pattern the epipods. To determine whether wings can be traced to ancestral, pre-insect structures, or arose by co-option, comparisons are necessary between insects and arthropods more representative of the ancestral state, where the hypothesized proximal leg region is not fused to the body wall. To do so, we examined the function of five leg patterning genes in the crustacean Parhyale hawaiensis and compared this to previous functional data from insects. By comparing gene knockout phenotypes of leg patterning genes in a crustacean with those of insects, we show that two ancestral crustacean leg segments were incorporated into the insect body, moving the legs epipod dorsally, up onto the back to form insect wings. Thus, our data shows that much of the body wall of insects, including the entire wing, is derived from these two ancestral proximal leg segments. This model explains all observations in favor of either the body wall origin or proximal leg origin of insect wings. Thus, our results show that insect wings are not novel structures, but instead evolved from existing, ancestral structures.\n\nOne Sentence SummaryCRISPR-Cas9 knockout of leg gap genes in a crustacean reveals that insect wings are not novel structures, they evolved from crustacean leg segments

developmental biology↗