Single locus affects embryonic segment polarity and multiple aspects of an adult evolutionary novelty

BMC Biology

Research Article

Suzanne V Saenko¹  Paul M Brakefield¹  Patrícia Beldade² 

[1] Institute of Biology, Leiden University, Sylviusweg 72, 2333, Leiden, BE, The Netherlands;Institute of Biology, Leiden University, Sylviusweg 72, 2333, Leiden, BE, The Netherlands;Instituto Gulbenkian de Ciência, Rua da Quinta Grande 6, P-2780-156, Oeiras, Portugal;

关键词: Mutant Embryo;    Wing Pattern;    Segment Polarity;    Evolutionary Developmental Biology;    Lethal Allele;   

DOI  :  10.1186/1741-7007-8-111

 received in 2010-06-30, accepted in 2010-08-26,  发布年份 2010

来源: Springer

【 摘 要 】

BackgroundThe characterization of the molecular changes that underlie the origin and diversification of morphological novelties is a key challenge in evolutionary developmental biology. The evolution of such traits is thought to rely largely on co-option of a toolkit of conserved developmental genes that typically perform multiple functions. Mutations that affect both a universal developmental process and the formation of a novelty might shed light onto the genetics of traits not represented in model systems. Here we describe three pleiotropic mutations with large effects on a novel trait, butterfly eyespots, and on a conserved stage of embryogenesis, segment polarity.ResultsWe show that three mutations affecting eyespot size and/or colour composition in Bicyclus anynana butterflies occurred in the same locus, and that two of them are embryonic recessive lethal. Using surgical manipulations and analysis of gene expression patterns in developing wings, we demonstrate that the effects on eyespot morphology are due to changes in the epidermal response component of eyespot induction. Our analysis of morphology and of gene expression in mutant embryos shows that they have a typical segment polarity phenotype, consistent with the mutant locus encoding a negative regulator of Wingless signalling.ConclusionsThis study characterizes the segregation and developmental effects of alleles at a single locus that controls the morphology of a lineage-specific trait (butterfly eyespots) and a conserved process (embryonic segment polarity and, specifically, the regulation of Wingless signalling). Because no gene with such function was found in the orthologous, highly syntenic genomic regions of two other lepidopterans, we hypothesize that our locus is a yet undescribed, possibly lineage-specific, negative regulator of the conserved Wnt/Wg pathway. Moreover, the fact that this locus interferes with multiple aspects of eyespot morphology and maps to a genomic region containing key wing pattern loci in different other butterfly species suggests it might correspond to a 'hotspot' locus in the diversification of this novel trait.

【 授权许可】

Unknown   
© Saenko et al; licensee BioMed Central Ltd. 2010. This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.