Over-expression of Ultrabithorax alters embryonic body plan and wing patterns in the butterfly Bicyclus anynana

Tong, Xiaoling; Hrycaj, Steven; Podlaha, Ondřej; Popadić, Aleksandar; Monteiro, Antónia

doi:10.1016/j.ydbio.2014.08.020

Cited by 46 publications

(55 citation statements)

References 41 publications

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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%

“…Dpp mRNA is expressed in regions around the developing eyespots in mid to late larval wings (Connahs et al 2019) in anti-colocalized patterns to Armadillo, a transcription factor effector of the Wingless signaling pathway. Armadillo is expressed in the actual eyespot centers in late larval stages (Connahs et al 2019), as is Antennapedia ( Antp ; BANY.1.2.g02571), a hox gene (Saenko et al 2011; Tong et al 2014; Özsu and Monteiro 2017). Antp is also involved in the differentiation of the thoracic limbs in Bombyx moths (Chen et al 2013).…”

Section: Discussionmentioning

confidence: 99%

“…Antp is also involved in the differentiation of the thoracic limbs in Bombyx moths (Chen et al 2013). Ultrabithorax ( Ubx ; BANY.1.2.g02579) is another hox gene that gives insect hindwings a different identity from forewings (Weatherbee et al 1999; Tong et al 2014). In B. anynana , this gene is expressed across the whole hindwing, a conserved expression pattern observed across insects, but has additional, stronger, expression in the eyespot centers of the hindwing only, something that is not seen in other butterflies with eyespots such as Junonia coenia (Tong et al 2014).…”

Section: Discussionmentioning

confidence: 99%

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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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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Multiple loci control eyespot number variation on the hindwings ofBicyclus anynanabutterflies

Rivera‐Colón

Westerman

Belleghem

et al. 2019

Preprint

Self Cite

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“…mori embryos at stage 20 were dissected and fixed in 4% paraformaldehyde for 30 min at 4°C. After fixation, the samples were washed in wash buffer (pH 6.8, 50 mM Tris, 150 mM NaCl, 0.5% (octylphenoxy) polyethoxyethanol (IGEPALCA-630), 1 mg/ml bovine serum albumin) and then incubated overnight at 4°C in a 1:200 dilution of anti-Dll [28]. The specimens were then incubated in a 1:1000 dilution of secondary antibody (Alexa Fluor 488, Beyotime) for 3h at 4°C.…”

Section: Methodsmentioning

confidence: 99%

Fine Mapping of a Degenerated Abdominal Legs Mutant (Edl) in Silkworm, Bombyx mori

et al. 2017

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In insects, abdominal appendages, also called prolegs, vary due to adaptive evolution. Mutations on prolegs within species provide insights to better understand the mechanisms underlying appendage development and diversity. In silkworm Bombyx mori, extra-crescents and degenerated abdominal legs (Edl) mutant, belonging to the E pseudoallele group, is a spontaneous mutation that adds crescents and degenerates prolegs on the third abdominal segment (A3). This mutation may be a homeotic transformation of A3 to A2. In this study, the Edl locus was mapped within approximately a 211 Kb region that is 10 Kb upstream of Bmabdominal-A (Bmabd-A). RT-quantitative PCR (RT-qPCR) and Western blot analysis of Bmabd-A expression showed a slight but significant decrease, while the expression of BmUltrabithorax (BmUbx) was up-regulated in the Edl mutant compared to wildtype (Dazao). Moreover, we also found that BmDistal-less (BmDll), which regulated the development of distal proleg structures, was missing at the tips of the A3 prolegs in the Edl mutant compared to BmDll expression in normally developed prolegs in both the wildtype and mutant. Collectively, we identified approximately a 211 Kb region in the Edl locus that regulates BmUbx and Bmabd-A expression and found that changes in BmUbx and Bmabd-A expression may lead to the loss of distal proleg structures in B. mori.

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“…Clones of cells lacking Ubx within an eyespot field lead to over-expression of Dll and subsequent alterations in the size of the hindwing eyespots relative to their forewing counterparts (Weatherbee et al, 1999). Additionally, ectopic expression of Ubx on the pupal wings of B. anynana activates the black-scale associated genes sal and Dll, and leads to the differentiation of black wing scales (Tong et al, 2014).…”

Section: Dll Regulation and Downstream Targetsmentioning

confidence: 99%

Distal-lesshomeobox genes of insects and spiders: genomic organization, function, regulation and evolution

2016

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The Distal-less (Dll) genes are homeodomain transcription factors that are present in most Metazoa and in representatives of all investigated arthropod groups. In Drosophila, the best studied insect, Dll plays an essential role in forming the proximodistal axis of the legs, antennae and analia, and in specifying antennal identity. The initiation of Dll expression in clusters of cells in mid-lateral regions of the Drosophila embryo represents the earliest genetic marker of limbs. Dll genes are involved in the development of the peripheral nervous system and sensitive organs, and they also function as master regulators of black pigmentation in some insect lineages. Here we analyze the complete genomes of six insects, the nematode Caenorhabditis elegans and Homo sapiens, as well as multiple Dll sequences available in databases in order to examine the structure and protein features of these genes. We also review the function, expression, regulation and evolution of arthropod Dll genes with emphasis on insects and spiders.

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Over-expression of Ultrabithorax alters embryonic body plan and wing patterns in the butterfly Bicyclus anynana

Cited by 46 publications

References 41 publications

Multiple loci control eyespot number variation on the hindwings ofBicyclus anynanabutterflies

Multiple loci control eyespot number variation on the hindwings ofBicyclus anynanabutterflies

Fine Mapping of a Degenerated Abdominal Legs Mutant (Edl) in Silkworm, Bombyx mori

Distal-lesshomeobox genes of insects and spiders: genomic organization, function, regulation and evolution

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