A Survey of Eyespot Sexual Dimorphism across Nymphalid Butterflies

Tokita, Christopher K.; Oliver, Jeffrey C.; Monteiro, Antónia

doi:10.1155/2013/926702

Cited by 16 publications

(20 citation statements)

References 17 publications

(19 reference statements)

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“…Many butterfly wings harbor an eyespot [ 16 , 17 ], which is a color pattern element that is especially well developed in nymphalid butterflies. Likely because of their concentric structures and their conspicuity, nymphalid eyespots have attracted developmental biologists.…”

Section: Introductionmentioning

confidence: 99%

Live Cell Imaging of Butterfly Pupal and Larval Wings In Vivo

Ohno

Otaki

2015

PLoS ONE

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Butterfly wing color patterns are determined during the late larval and early pupal stages. Characterization of wing epithelial cells at these stages is thus critical to understand how wing structures, including color patterns, are determined. Previously, we successfully recorded real-time in vivo images of developing butterfly wings over time at the tissue level. In this study, we employed similar in vivo fluorescent imaging techniques to visualize developing wing epithelial cells in the late larval and early pupal stages 1 hour post-pupation. Both larval and pupal epithelial cells were rich in mitochondria and intracellular networks of endoplasmic reticulum, suggesting high metabolic activities, likely in preparation for cellular division, polyploidization, and differentiation. Larval epithelial cells in the wing imaginal disk were relatively large horizontally and tightly packed, whereas pupal epithelial cells were smaller and relatively loosely packed. Furthermore, larval cells were flat, whereas pupal cells were vertically elongated as deep as 130 μm. In pupal cells, many endosome-like or autophagosome-like structures were present in the cellular periphery down to approximately 10 μm in depth, and extensive epidermal feet or filopodia-like processes were observed a few micrometers deep from the cellular surface. Cells were clustered or bundled from approximately 50 μm in depth to deeper levels. From 60 μm to 80 μm in depth, horizontal connections between these clusters were observed. The prospective eyespot and marginal focus areas were resistant to fluorescent dyes, likely because of their non-flat cone-like structures with a relatively thick cuticle. These in vivo images provide important information with which to understand processes of epithelial cell differentiation and color pattern determination in butterfly wings.

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Section: Introductionmentioning

confidence: 99%

Live Cell Imaging of Butterfly Pupal and Larval Wings In Vivo

Ohno

Otaki

2015

PLoS ONE

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“…Changes may still occur before final publication online and in print the majority of cases females display more eyespots; in the minority males do. In addition, dorsal surfaces of both forewings and hindwings and ventral surfaces of forewings display relatively few eyespots but are disproportionately more sexually dimorphic than ventral hindwing surfaces (78). Sexual dimorphism in eyespots can result either from natural selection acting differentially in each sex, as shown recently in Junonia evarete (63), or from the action of sexual selection, as observed in B. anynana (65,66,86).…”

Section: Monteiromentioning

confidence: 80%

“…A recent survey of presence and absence of eyespots across nearly 450 nymphalids found a large degree of sexual dimorphism in these traits: Nearly 80% of the species with eyespots (278) were sexually dimorphic for eyespot number (78). The sexual dimorphism happens in two directions: In…”

Section: Evolution Of Eyespot Number Morphology and Sexual Dimorphismmentioning

confidence: 99%

Origin, Development, and Evolution of Butterfly Eyespots

Monteiro

2015

Annu. Rev. Entomol.

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100

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This article reviews the latest developments in our understanding of the origin, development, and evolution of nymphalid butterfly eyespots. Recent contributions to this field include insights into the evolutionary and developmental origin of eyespots and their ancestral deployment on the wing, the evolution of eyespot number and eyespot sexual dimorphism, and the identification of genes affecting eyespot development and black pigmentation. I also compare features of old and more recently proposed models of eyespot development and propose a schematic for the genetic regulatory architecture of eyespots. Using this schematic I propose two hypotheses for why we observe limits to morphological diversity across these serially homologous traits.

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“…Eyespots originally appeared on the ventral hindwing in a lineage of nymphalid butterflies, sister to the Danainae, and have subsequently been added to the forewings and dorsal surfaces of both wings (Oliver et al 2012, 2014; Schachat et al 2015). Furthermore, within a single species, eyespot number can vary significantly between individuals or sexes (Brakefield and van Noordwijk 1985; Owen 1993; Tokita et al 2013), allowing for population genetic approaches to identify the underlying genetic basis of such variation. Genes controlling eyespot number variation within a species might also be involved in promoting this type of variation across species.…”

Section: Introductionmentioning

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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A Survey of Eyespot Sexual Dimorphism across Nymphalid Butterflies

Cited by 16 publications

References 17 publications

Live Cell Imaging of Butterfly Pupal and Larval Wings In Vivo

Live Cell Imaging of Butterfly Pupal and Larval Wings In Vivo

Origin, Development, and Evolution of Butterfly Eyespots

Multiple loci control eyespot number variation on the hindwings ofBicyclus anynanabutterflies

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