Wound healing, calcium signaling, and other novel pathways are associated with the formation of butterfly eyespots

Özsu, Nesibe; Monteiro, Antónia

doi:10.1186/s12864-017-4175-7

Cited by 41 publications

(61 citation statements)

References 113 publications

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“…Transcriptome analyses revealed that a surprisingly large number of genes were specifically regulated in the area of pigmentation formation: 78 genes were upregulated commonly in the pigmentation area and by wingless, and 73 genes were downregulated commonly in the pigmentation area and by wingless. In the butterfly Bicyclus anynana, 132 genes were upregulated and 54 genes were downregulated in relation to eye spot formation [24]. In comparison with these numbers of genes in butterflies, the number of genes identified by our results seem reasonable.…”

Section: A Large Number Of Genes Were Specifically Regulated In the Asupporting

confidence: 53%

“…There is an ongoing discussion about whether a large gene circuit is recruited or many genes are individually recruited to form a circuit during the evolution of a novel trait [41,42]. Examples of co-option of pre-existing circuits consisting of multiple regulatory genes are known from animals and plants [11,24,[43][44][45][46]. In the present case, we can ask whether the large gene network for pigmentation regulated by a master control gene, wingless, was co-opted all at the same time, or whether individual genes were co-opted one by one to form the current network.…”

Section: Evolutionary Scenario Of Pigmentation Pattern Evolutionmentioning

confidence: 99%

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Transcriptome analysis reveals evolutionary co-option of neural development and signaling genes for the wing pigmentation pattern of the polka-dotted fruit fly

Fukutomi

Kondo

Toyoda

et al. 2020

Preprint

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How evolutionary novelties have arisen is one of the central questions in evolutionary biology. Pre-existing gene regulatory networks or signaling pathways have been shown to be co-opted for building novel traits in several organisms. However, the structure of entire gene regulatory networks and evolutionary events of gene co-option for emergence of a novel trait are poorly understood. In this study, we used a novel wing pigmentation pattern of the polka-dotted fruit fly, and identified the complete set of genes for pigmentation pattern formation by de novo genome sequencing and transcriptome analyses. In pigmentation areas of wings, 151 genes were positively or negatively regulated by wingless, a master regulator of wing pigmentation. Genes for neural development, Wnt signaling, Dpp signaling, Zinc finger transcription factors, and effectors (such as enzymes) for melanin pigmentation were included among these 151 genes. None of the known regulatory genes that regulate pigmentation pattern formation in other fruit fly species were included. Our results suggest that the novel pigmentation pattern of the polka-dotted fruit fly emerged through multi-step co-options of multiple gene regulatory networks, signaling pathways, and effector genes, rather than recruitment of one large gene circuit.

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Section: A Large Number Of Genes Were Specifically Regulated In the Asupporting

confidence: 53%

Section: Evolutionary Scenario Of Pigmentation Pattern Evolutionmentioning

confidence: 99%

Transcriptome analysis reveals evolutionary co-option of neural development and signaling genes for the wing pigmentation pattern of the polka-dotted fruit fly

Fukutomi

Kondo

Toyoda

et al. 2020

Preprint

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“…Among our identified candidates, we observed a total of seven genes previously implicated in eyespot development in B. anynana : CDase, Dpp, Antp, Ubx, Sal3, Cd63 , and Syntaxin 7 (Brunetti et al 2001; Tong et al 2014; Özsu and Monteiro 2017; Connahs et al 2019) (Table 2). From these, only dpp and Cd63 remained associated at the highest significant threshold of 7 SD.…”

Section: Discussionmentioning

confidence: 99%

“…Most of these genes are within or near the area of strongest association, and only Cd63 has an associated SNP within an intron (Table 3 and Figure 4). Neutral Ceramidase ( CDase ; BANY.1.2.g00030) is an enzyme involved in the metabolism of sphingolipids which is down-regulated in eyespots relative to flanking wing tissue (Özsu and Monteiro 2017). Sphingolipids appear to function in a variety of cell signaling pathways but are still poorly understood (Hannun and Obeid 2017).…”

Section: Discussionmentioning

confidence: 99%

Multiple loci control eyespot number variation on the hindwings ofBicyclus anynanabutterflies

Rivera‐Colón

Westerman

Belleghem

et al. 2019

Preprint

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27The underlying genetic changes that regulate the appearance and disappearance of 28 repeated traits, or serial homologs, remain poorly understood. One hypothesis is 29 that variation in genomic regions flanking master regulatory genes, also known as 30 input-output genes, controls variation in trait number, making the locus of 31 evolution almost predictable. Other hypotheses implicate genetic variation in up-32 stream or downstream loci of master control genes. Here, we use the butterfly 33Bicyclus anynana, a species which exhibits natural variation in eyespot number 34 on the dorsal hindwing, to test these two hypotheses. We first estimated the 35 heritability of dorsal hindwing eyespot number by breeding multiple butterfly 36 families differing in eyespot number, and regressing eyespot number of offspring 37 on mid-parent values. We then estimated the number and identity of independent 38 genetic loci contributing to eyespot number variation by performing a genome-39 wide association study with restriction site-associated DNA Sequencing (RAD-seq) 40 from multiple individuals varying in number of eyespots sampled across a freely 41 breeding lab population. We found that dorsal hindwing eyespot number has a 42 moderately high heritability of approximately 0.50. In addition, multiple loci near 43 previously identified genes involved in eyespot development display high 44 association with dorsal hindwing eyespot number, suggesting that homolog 45 number variation is likely determined by regulatory changes at multiple loci that 46 build the trait and not by variation at single master regulators or input-output 47 49 Body plans often evolve through changes in the number of repeated parts or serial 50 homologs by either addition or subtraction. For instance, the pelvic fins of 51 vertebrates are inferred to have originated by addition to a body plan displaying 52 only pectoral fins, perhaps via co-option of the pectoral or caudal fin 53 developmental programs to a novel location in the body (Ruvinsky and Gibson-54 Brown 2000; Larouche et al. 2017). In insects, the absence of limbs and wings in 55 the abdomen is inferred to be due to a process of subtraction, i.e. via the repression 56 or modification of limbs and wings in these segments by hox genes (Galant and 57 Carroll 2002; Ronshaugen et al. 2002; Tomoyasu et al. 2005; Ohde et al. 2013). 58 Regulatory targets of abdominal hox genes are likely to underlie loss of limb/wing 59 number in these body segments (Tomoyasu et al. 2005; Ohde et al. 2013), 60 although these mutations have not yet been identified. Thus, while serial homolog 61 number variation is a common feature in the evolution of organisms' body plans, 62 the underlying genetic changes that regulate the appearance and disappearance of 63 these repeated traits remain poorly understood. 64 65 Studies in Drosophila have contributed most to the identification of the genetic 66 basis underlying the evolution of serial homolog number. Larvae of different 67 species have different numbers of small hairs, or tr...

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“…Intercellular calcium waves transmit local information from the initiator cell to a large number of cells in order to coordinate and synchronize their activity during development (Moreno-Juan et al, 2017;Akahoshi , Hotta and Oka 2017, Wallingford et al 2001, Webb and Miller 2003, Özsu and Monteiro 2017. Surprisingly, endogenous calcium waves during embryogenesis of insects have not been documented.…”

Section: Introductionmentioning

confidence: 99%

Spatiotemporal dynamics of calcium transients during embryogenesis of Drosophila melanogaster

Markova

Senatore

Lenne

2019

Preprint

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Calcium signaling plays a crucial role in the physiology of the organs but also in various aspects of the organogenesis of the embryo. High versatility of calcium signaling is encoded by the dynamic variation of intracellular calcium concentration. While the dynamics of calcium is important, little is known about it throughout the embryogenesis of the largest class of animals, insects. Here, we visualize calcium dynamics throughout embryogenesis of Drosophila using a fluorescent proteinbased calcium indicator, GCaMP3, and report calcium transients in epithelium and neuronal tissues. Local calcium transients of varying duration were detected in the outer epithelium, trachea and neural cells. In addition, gap-junction-dependent calcium waves were identified at stage 16 in the outer epithelium and in the trachea at stage 17. Calcium transient waveform analysis revealed different characteristics as a function of the duration, location and frequency. Detailed characterization of calcium transients during embryogenesis of Drosophila will help us better understand the role of calcium signaling in embryogenesis and organogenesis of insects.

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Wound healing, calcium signaling, and other novel pathways are associated with the formation of butterfly eyespots

Cited by 41 publications

References 113 publications

Transcriptome analysis reveals evolutionary co-option of neural development and signaling genes for the wing pigmentation pattern of the polka-dotted fruit fly

Transcriptome analysis reveals evolutionary co-option of neural development and signaling genes for the wing pigmentation pattern of the polka-dotted fruit fly

Multiple loci control eyespot number variation on the hindwings ofBicyclus anynanabutterflies

Spatiotemporal dynamics of calcium transients during embryogenesis of Drosophila melanogaster

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