Abstract
BackgroundHox proteins specify segment identity during embryogenesis and have typical associated expression patterns. Changes in embryonic expression and activity of Hox genes were crucial in the evolution of animal body plans, but their role in the post-embryonic development of lineage-specific traits remains largely unexplored. Here, we focus on the insect Hox genes Ultrabithorax (Ubx) and Antennapedia (Antp), and implicate the latter in the formation and diversification of novel, butterfly-specific wing patterns.ResultsFirst, we describe a conserved pattern of Ubx expression and a novel pattern of Antp expression in wing discs of Bicyclus anynana butterflies. The discrete, reiterated domains of Antp contrast with the typical expression of Hox genes in single continuous regions in arthropod embryos. Second, we show that this pattern is associated with the establishment of the organizing centres of eyespots. Antp upregulation is the earliest event in organizer development described to date, and in contrast to all genes implicated in eyespot formation, is exclusive to those centres. Third, our comparative analysis of gene expression across nymphalids reveals unexpected differences in organizer determination.ConclusionsWe show that the Antp's recruitment for the formation of novel traits in butterfly wing discs involved the evolution of new expression domains, and is restricted to a particular lineage. This study contributes novel insights into the evolution of Antp expression, as well as into the genetic mechanisms underlying morphological diversification. Our results also underscore how a wider representation of morphological and phylogenetic diversity is essential in evolutionary developmental biology.
Highlights
Hox proteins specify segment identity during embryogenesis and have typical associated expression patterns
The fact that Ubx is expressed ubiquitously on the hindwing with no association to any particular wing regions suggests that this Hox gene, for which changes in expression have been associated with colour pattern transformations in J. coenia [13], is not involved in the determination of any specific colour pattern element in B. anynana
To our knowledge, such an expression pattern is novel for Antp, which was never before detected in the developing insect wing blade, nor in a series of discrete and reiterated domains
Summary
Hox proteins specify segment identity during embryogenesis and have typical associated expression patterns. We focus on the insect Hox genes Ultrabithorax (Ubx) and Antennapedia (Antp), and implicate the latter in the formation and diversification of novel, butterfly-specific wing patterns. In the past two decades, multiple studies revealed that novelties often evolve through “teaching old genes new tricks”, as shared genes and/or gene regulatory networks become co-opted to perform new functions during development (reviewed in [5,6,7,8]) Such recruitment can occur via the acquisition of new expression domains, as has been shown for insect appendage patterning genes redeployed for the development of head/pronotum horns in beetles [9], abdominal legs in sepsid flies [10], and wing eyespots in butterflies [11]. We investigated the involvement of Ubx and Antp in the development and diversification of butterfly colour patterns that start to be established in larval wing discs
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