Nymphalid eyespots are co-opted to novel wing locations following a similar pattern in independent lineages.

Sandra R Schachat,Jeffrey C Oliver,Antónia Monteiro

doi:10.1186/s12862-015-0300-x

Abstract

BackgroundVariation in the number of repeated traits, or serial homologs, has contributed greatly to animal body plan diversity. Eyespot color patterns of nymphalid butterflies, like arthropod and vertebrate limbs, are an example of serial homologs. These eyespot color patterns originated in a small number of wing sectors on the ventral hindwing surface and later appeared in novel wing sectors, novel wings, and novel wing surfaces. However, the details of how eyespots were co-opted to these novel wing locations are currently unknown.ResultsWe used a large data matrix of eyespot/presence absence data, previously assembled from photographs of contemporary species, to perform a phylogenetic investigation of eyespot origins in nine independent nymphalid lineages. To determine how the eyespot gene regulatory network acquired novel positional information, we used phylogenetic correlation analyses to test for non-independence in the origination of eyespots. We found consistent patterns of eyespot gene network redeployment in the nine lineages, where eyespots first redeployed from the ventral hindwing to the ventral forewing, then to new sectors within the ventral wing surface, and finally to the dorsal wing surface. Eyespots that appeared in novel wing sectors modified the positional information of their serial homolog ancestors in one of two ways: by changing the wing or surface identity while retaining sector identity, or by changing the sector identity while retaining wing and surface identity.ConclusionsEyespot redeployment to novel sectors, wings, and surfaces happened multiple times in different nymphalid subfamilies following a similar pattern. This indicates that parallel mutations altering expression of the eyespot gene regulatory network led to its co-option to novel wing locations over time.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0300-x) contains supplementary material, which is available to authorized users.

Highlights

Variation in the number of repeated traits, or serial homologs, has contributed greatly to animal body plan diversity
Within the ventral wing surface, we found the origin of some eyespots on the forewing (M3 and Cu1, and possibly R5, M1, and M2) to be contingent on the presence of an eyespot in the homologous sector on the hindwing (Figure 5; Additional file 4: Table S2); in contrast, origins of eyespots on the ventral hindwing were not contingent on the presence of eyespots on the ventral forewing, nor were dorsal eyespot origins on either wing contingent on the presence of eyespots on the other wing
Eyespots in sectors ScR, Cu2, and Pc belong to the third category, where eyespots are redeployed to different wing sectors within a single wing surface (Figure 6B): our results indicate that these eyespots originate from modifications of positional information coding for eyespots present in other sectors on the same wing

Summary

Introduction

Variation in the number of repeated traits, or serial homologs, has contributed greatly to animal body plan diversity. Show that Nymphalid eyespots originated during the late Cretaceous in a few sectors on the ventral surface of the Schachat et al BMC Evolutionary Biology (2015) 15:20 required to deploy eyespots to new locations. By evaluating these models in multiple lineages of nymphalid butterflies we can assess the degree to which there are shared pathways by which novel positional information evolves to generate diversity in butterfly eyespot number and location

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