scholarly journals Two sets of wing homologs in the crustacean, Parhyale hawaiensis

2017 ◽  
Author(s):  
Courtney M. Clark-Hachtel ◽  
Yoshinori Tomoyasu
Keyword(s):  
Genome Editing ◽  
Regulatory Network ◽  
Body Wall ◽  
Ancestral State ◽  
Insect Wing ◽  
Insect Wings ◽  
Parhyale Hawaiensis ◽  
Gene Regulatory ◽  
Competing Hypotheses ◽  
Dual Origin

The origin of insect wings is a biological mystery that has fascinated scientists for centuries. Through extensive investigations performed across various fields, two possible wing origin tissues have been identified; a lateral outgrowth of the dorsal body wall (tergum) and ancestral proximal leg structures1,2. With each idea offering both strengths and weaknesses, these two schools of thought have been in an intellectual battle for decades without reaching a consensus3. Identification of tissues homologous to insect wings from linages outside of Insecta will provide pivotal information to resolve this conundrum. Here, through expression analyses and CRISPR/Cas9-based genome-editing in the crustacean, Parhyale hawaiensis, we show that a wing-like gene regulatory network (GRN) operates both in the crustacean terga and in the proximal leg segments, suggesting that (i) the evolution of a wing-like GRN precedes the emergence of insect wings, and (ii) that both of these tissues are equally likely to be crustacean wing homologs. Interestingly, the presence of two sets of wing homologs parallels previous findings in some wingless segments of insects, where wing serial homologs are maintained as two separate tissues4–7. This similarity provides crucial support for the idea that the wingless segments of insects indeed reflect an ancestral state for the tissues that gave rise to the insect wing, while the true insect wing represents a derived state that depends upon the contribution of two distinct tissues. These outcomes point toward a dual origin of insect wings, and thus provide a crucial opportunity to unify the two historically competing hypotheses on the origin of this evolutionarily monumental structure.

scholarly journals Wing serial homologues and the diversification of insect outgrowths: insights from the pupae of scarab beetles

2021 ◽  
Vol 288 (1943) ◽  
pp. 20202828
Author(s):  
Yonggang Hu ◽  
Armin P. Moczek
Keyword(s):  
Regulatory Network ◽  
Body Wall ◽  
Life Stages ◽  
Support Structures ◽  
Developmental Evolution ◽  
Insect Wings ◽  
Gene Regulatory ◽  
Focal Structures ◽  
Compare And Contrast ◽  
Scarab Beetles

Modification of serially homologous structures is a common avenue towards functional innovation in developmental evolution, yet ancestral affinities among serial homologues may be obscured as structure-specific modifications accumulate over time. We sought to assess the degree of homology to wings of three types of body wall projections commonly observed in scarab beetles: (i) the dorsomedial support structures found on the second and third thoracic segments of pupae, (ii) the abdominal support structures found bilaterally in most abdominal segments of pupae, and (iii) the prothoracic horns which depending on species and sex may be restricted to pupae or also found in adults. We functionally investigated 14 genes within, as well as two genes outside, the canonical wing gene regulatory network to compare and contrast their role in the formation of each of the three presumed wing serial homologues. We found 11 of 14 wing genes to be functionally required for the proper formation of lateral and dorsal support structures, respectively, and nine for the formation of prothoracic horns. At the same time, we document multiple instances of divergence in gene function across our focal structures. Collectively, our results support the hypothesis that dorsal and lateral support structures as well as prothoracic horns share a developmental origin with insect wings. Our findings suggest that the morphological and underlying gene regulatory diversification of wing serial homologues across species, life stages and segments has contributed significantly to the extraordinary diversity of arthropod appendages and outgrowths.

scholarly journals The Daphnia Carapace and the Origin of Novel Structures

2021 ◽  
Author(s):  
Heather Bruce
Keyword(s):  
General Solution ◽  
Body Wall ◽  
Lateral Lobe ◽  
Central Question ◽  
Insect Wing ◽  
Insect Wings ◽  
Positive Region ◽  
Novel Structure ◽  
Novel Structures

Understanding how novel structures arise is a central question in evolution. The carapace of the waterflea Daphnia is a bivalved “cape” of exoskeleton that surrounds the animal, and has been proposed to be one of many novel structures that arose through repeated co-option of genes that also pattern insect wings. To determine whether the Daphnia carapace is a novel structure, the expression of pannier, the Iroquois gene aurucan, and vestigial are compared between Daphnia, Parhyale, and Tribolium. The results suggest that the Daphnia carapace did not arise by cooption, but instead represents an elongated ancestral exite (lateral lobe or plate) that emerges from a 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 wing. In addition, the vg-positive region that gives rise to the Daphnia carapace also appears to be present in Parhyale and Tribolium, which do not form a carapace. Thus, rather than a novel structure resulting from gene co-option, the carapace appears to have arisen from an ancient, conserved developmental field that persists in a cryptic state in other arthropod lineages, but in Daphnia became elaborated into the carapace. Cryptic persistence of serially homologous developmental fields may thus be a general solution for the origin of many novel structures.

scholarly journals The Daphnia Carapace and the Origin of Novel Structures

2021 ◽  
Author(s):  
Heather Bruce
Keyword(s):  
General Solution ◽  
Body Wall ◽  
Lateral Lobe ◽  
Central Question ◽  
Insect Wing ◽  
Insect Wings ◽  
Positive Region ◽  
Novel Structure ◽  
Novel Structures

Understanding how novel structures arise is a central question in evolution. The carapace of the waterflea Daphnia is a bivalved “cape” of exoskeleton that surrounds the animal, and has been proposed to be one of many novel structures that arose through repeated co-option of genes that also pattern insect wings. To determine whether the Daphnia carapace is a novel structure, the expression of pannier, the Iroquois gene aurucan, and vestigial are compared between Daphnia, Parhyale, and Tribolium. The results suggest that the Daphnia carapace did not arise by cooption, but instead represents an elongated ancestral exite (lateral lobe or plate) that emerges from a 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 wing. In addition, the vg-positive region that gives rise to the Daphnia carapace also appears to be present in Parhyale and Tribolium, which do not form a carapace. Thus, rather than a novel structure resulting from gene co-option, the carapace appears to have arisen from an ancient, conserved developmental field that persists in a cryptic state in other arthropod lineages, but in Daphnia became elaborated into the carapace. Cryptic persistence of serially homologous developmental fields may thus be a general solution for the origin of many novel structures.

scholarly journals The Daphnia carapace and the origin of novel structures

2021 ◽  
Author(s):  
Heather S. Bruce ◽  
Nipam H. Patel
Keyword(s):  
General Solution ◽  
Body Wall ◽  
Lateral Lobe ◽  
Central Question ◽  
Insect Wing ◽  
Functional Studies ◽  
Insect Wings ◽  
Positive Region ◽  
Novel Structure ◽  
Novel Structures

SummaryUnderstanding how novel structures arise is a central question in evolution. The carapace of the waterflea Daphnia 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 wings1–3. 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 ancestral exite (lateral lobe) that emerges from a 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 wing4. Remarkably, the vestigial-positive region that gives rise to the Daphnia carapace appears to be present in Parhyale5 and Tribolium as a small, inconspicuous protrusion. Similarly, the vestigial-positive developmental fields that form tergal plates in Parhyale appear to be present in Daphnia, even though Daphnia does not form tergal plates. Thus, rather than a novel structure resulting from gene co-option, the Daphnia carapace appears to have arisen from a shared, ancestral developmental field that persists in a cryptic state in other arthropod lineages. Cryptic persistence of unrecognized serially homologous developmental fields may thus be a general solution for the origin of novel structures. Our simple molecular triangulation strategy, which does not require functional studies, can illuminate the homologies of long-debated structures on the legs and body wall of arthropods.

scholarly journals A genome-wide assessment of the ancestral neural crest gene regulatory network

2018 ◽  
Author(s):  
Dorit Hockman ◽  
Vanessa Chong-Morrison ◽  
Daria Gavriouchkina ◽  
Stephen Green ◽  
Chris T. Amemiya ◽  
...  
Keyword(s):  
Neural Crest ◽  
Gene Regulatory Network ◽  
Regulatory Network ◽  
Regulatory Elements ◽  
Ancestral State ◽  
Enhancer Activity ◽  
Mesenchymal Transition ◽  
A Genome ◽  
Gene Regulatory ◽  
Insight Into

AbstractThe neural crest is an embryonic cell population that contributes to key vertebrate-specific features including the craniofacial skeleton and peripheral nervous system. Here we examine the transcriptional profiles and chromatin accessibility of neural crest cells in the basal sea lamprey, in order to gain insight into the ancestral state of the neural crest gene regulatory network (GRN) at the dawn of vertebrates. Transcriptome analyses reveal clusters of co-regulated genes during neural crest specification and migration that show high conservation across vertebrates for dynamic programmes like Wnt modulation during the epithelial to mesenchymal transition, but also reveal novel transcription factors and cell-adhesion molecules not previously implicated in neural crest migration. ATAC-seq analysis refines the location of known cis-regulatory elements at the Hox-α2 locus and uncovers novel cis-regulatory elements for Tfap2B and SoxE1. Moreover, cross-species deployment of lamprey elements in zebrafish reveals that the lamprey SoxE1 enhancer activity is deeply conserved, mediating homologous expression in jawed vertebrates. Together, our data provide new insight into the core elements of the GRN that are conserved to the base of the vertebrates, as well as expose elements that are unique to lampreys.

scholarly journals A genome-wide assessment of the ancestral neural crest gene regulatory network

2019 ◽  
Vol 10 (1) ◽  
Author(s):  
Dorit Hockman ◽  
Vanessa Chong-Morrison ◽  
Stephen A. Green ◽  
Daria Gavriouchkina ◽  
Ivan Candido-Ferreira ◽  
...  
Keyword(s):  
Neural Crest ◽  
Gene Regulatory Network ◽  
Regulatory Network ◽  
Regulatory Elements ◽  
Embryonic Cell ◽  
Ancestral State ◽  
Enhancer Activity ◽  
A Genome ◽  
Gene Regulatory ◽  
Insight Into

Abstract The neural crest (NC) is an embryonic cell population that contributes to key vertebrate-specific features including the craniofacial skeleton and peripheral nervous system. Here we examine the transcriptional and epigenomic profiles of NC cells in the sea lamprey, in order to gain insight into the ancestral state of the NC gene regulatory network (GRN). Transcriptome analyses identify clusters of co-regulated genes during NC specification and migration that show high conservation across vertebrates but also identify transcription factors (TFs) and cell-adhesion molecules not previously implicated in NC migration. ATAC-seq analysis uncovers an ensemble of cis-regulatory elements, including enhancers of Tfap2B, SoxE1 and Hox-α2 validated in the embryo. Cross-species deployment of lamprey elements identifies the deep conservation of lamprey SoxE1 enhancer activity, mediating homologous expression in jawed vertebrates. Our data provide insight into the core GRN elements conserved to the base of the vertebrates and expose others that are unique to lampreys.

scholarly journals Out from under the wing: reconceptualizing the insect wing gene regulatory network as a versatile, general module for body-wall lobes in arthropods

2021 ◽  
Vol 288 (1965) ◽  
Author(s):  
Cera R. Fisher ◽  
Justin D. Kratovil ◽  
David R. Angelini ◽  
Elizabeth L. Jockusch
Keyword(s):  
Regulatory Network ◽  
Body Wall ◽  
Experimental Manipulation ◽  
The Body ◽  
Oncopeltus Fasciatus ◽  
Body Parts ◽  
Insect Wing ◽  
Wall Structures ◽  
New Perspective ◽  
And Function

Body plan evolution often occurs through the differentiation of serially homologous body parts, particularly in the evolution of arthropod body plans. Recently, homeotic transformations resulting from experimental manipulation of gene expression, along with comparative data on the expression and function of genes in the wing regulatory network, have provided a new perspective on an old question in insect evolution: how did the insect wing evolve? We investigated the metamorphic roles of a suite of 10 wing- and body-wall-related genes in a hemimetabolous insect, Oncopeltus fasciatus . Our results indicate that genes involved in wing development in O. fasciatus play similar roles in the development of adult body-wall flattened cuticular evaginations. We found extensive functional similarity between the development of wings and other bilayered evaginations of the body wall. Overall, our results support the existence of a versatile development module for building bilayered cuticular epithelial structures that pre-dates the evolutionary origin of wings. We explore the consequences of reconceptualizing the canonical wing-patterning network as a bilayered body-wall patterning network, including consequences for long-standing debates about wing homology, the origin of wings and the origin of novel bilayered body-wall structures. We conclude by presenting three testable predictions that result from this reconceptualization.

scholarly journals Insect wings and body wall evolved from ancient leg segments

2018 ◽  
Author(s):  
Heather S. Bruce ◽  
Nipam H. Patel
Keyword(s):  
Functional Data ◽  
Body Wall ◽  
Gene Knockout ◽  
The Body ◽  
Ancestral State ◽  
Gap Genes ◽  
Insect Wings ◽  
Patterning Genes ◽  
Novel Structures ◽  
Do So

AbstractThe 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 leg’s 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.One 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

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