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Nymphalid eyespots are co-opted to novel wing locations following a similar pattern in independent lineages Schachat, S. R., Oliver, J. C., & Monteiro, A. (2015). Nymphalid eyespots are co-opted to novel wing locations following a similar pattern in independent lineages. BMC Evolutionary Biology, 15, 20. doi:10.1186/s12862-015-0300-x 10.1186/s12862-015-0300-x BioMed Central Ltd. Version of Record http://cdss.library.oregonstate.edu/sa-termsofuse Schachat et al. BMC Evolutionary Biology (2015) 15:20 DOI 10.1186/s12862-015-0300-x RESEARCH ARTICLE Open Access Nymphalid eyespots are co-opted to novel wing locations following a similar pattern in independent lineages Sandra R Schachat1,2*, Jeffrey C Oliver3 and Antónia Monteiro4,5,6* Abstract Background: Variation 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. Results: We 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. Conclusions: Eyespot 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. Keywords: Serial homology, Correlation analysis, Ancestral states, Phylogeny, Wing patterns Background largely shared network [10]. However, in many of the ex- Animal bodies are often made up of repeated units, or amples above, it is still unclear how the gene regulatory serial homologs, which vary in number, size, shape, and network, responsible for the development of each serial position and largely contribute to body plan diversity. homolog, became deployed at each body location and Examples of serial homologs include vertebrate limbs [1] gained individuation from the other units to generate and teeth [2]; insect limbs [3], bristles [4,5], and tri- body plan diversity. chomes [6,7]; and nymphalid butterfly eyespots [8]. In Here we focus on unraveling the evolution of nym- many animal lineages, the development of serial homo- phalid butterfly eyespot number. Variation in eyespot logs and other complex traits is mediated via gene regu- number and position contributes to the morphological latory networks [9]. Serial homologs develop using a diversity of this clade (Figure 1). Earlier hypotheses, based on the nymphalid groundplan model [11], sug- * Correspondence: [email protected]; [email protected] gested that eyespot number diversity could have arisen 1Department of Biochemistry, Molecular Biology, Entomology and Plant from a primitive state where eyespots were present Pathology, Mississippi State University, Mississippi State, MS 39762, USA across all wing sectors [8,12]. Recent advances, however, 4Department of Ecology & Evolutionary Biology, Yale University, New Haven, CT 06520, USA show that Nymphalid eyespots originated during the late Full list of author information is available at the end of the article Cretaceous in a few sectors on the ventral surface of the © 2015 Schachat et al.; licensee BioMed Central. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Schachat et al. BMC Evolutionary Biology (2015) 15:20 Page 2 of 9 required to deploy eyespots to new locations. Further- more, 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 in- formation evolves to generate diversity in butterfly eye- spot number and location. Methods Data collection and ancestral state reconstructions We collected character data from 394 nymphalid species based on phylogenetic sampling of previous studies Figure 1 Examples of eyespot diversity in nymphalid [16,17]. The majority of specimens are from holdings in butterflies. (A) Hamanumida daedalus (YPM ENT 422238). the Yale Peabody Natural History Museum, the American (B) Hamadryas februa (YPM ENT 815633). (C) Marpesia eleuchea Museum of Natural History, and the Harvard Museum of (YPM ENT 815891). (D) Neorina crishna (YPM ENT 407679). (E) Bicyclus anynana (YPM ENT 814497). (F) Megisto cymela (YPM ENT 405705). All Comparative Zoology. For each species, we scored eyespot photographs show the ventral wing surface of female butterflies; all presence/absence for all wing surfaces (the dorsal and ven- specimens represent taxa investigated in this study and are housed in tral surfaces of the forewing and hindwing), for a grand the Entomology Collection of the Yale Peabody Museum of total of 38 different wing sectors for a single side of the Natural History. body (Additional file 1). We scored eyespots for each of the sexes, and used two specimens per sex when possible. An eyespot is defined as a circular pattern element con- hindwing [13,14]. This means that the eyespot gene taining two or more concentric rings of color [8]. Add- regulatory network originated with positional informa- itional pattern elements, such as patches and single-color tion coding for a particular wing (hindwing), a particular spots, were not used in these analyses. All patterns were surface (ventral surface), and particular sector identities scored from photographs available at www.lepdata.org. (Rs, M1, M2, M3, and Cu1). Subsequently, perhaps due We used the estimate of nymphalid phylogeny published to evolution in the regulation of key network genes by Wahlberg et al. [17]. [5,15], the network was redeployed in novel wings, sur- faces, and wing sectors [13,14], but the details of these Identification of independent clades for analysis redeployments have not yet been described. We analyzed eyespot number evolution separately across Here we take a phylogenetic approach to examine how nine clades, belonging to five different subfamilies of eyespots evolved at novel wing locations. We used correl- Nymphalidae (Figure 2). The number of eyespots present ation analyses to elucidate patterns of independence and on female butterflies was totaled for each species non-independence across pairs of eyespots, and there- sampled. We identified the top 50 species with the high- fore, the patterns of eyespot deployment on the wing. est number of eyespots (13 or more). Of these 50 spe- We used ancestral state reconstructions to evaluate an it- cies, 18 are interspersed through 18 different clades. The erative series of eyespot evolution models, allowing tests other 32 are clustered into 9 clades, each of which con- of potential pathways through which eyespots may be de- tains at least two species with 13 or more eyespots ployed across different wing locations. These models pro- (Additional file 2: Table S1; Figure 2). For each clade, vide a test for whether the origin of an eyespot in one separate eyespot presence/absence matrices were wing location is contingent on the presence of another retained for each eyespot in both males and females, for eyespot in a different wing location. Comparison among a total of 76 matrices per clade. Sexes were analyzed separately. models of evolutionary change thus allow us to evaluate support for the possibility that regulatory information Eyespot models of evolution coding for the more recent (i.e. “derived”) eyespot For each clade, we restricted our analyses to those pairs evolved from regulatory information that coded for the of eyespots that were inferred to have a shared history in older (i.e. “ancestral”) eyespot. In contrast, those cases in the clade being investigated. A shared history was in- which eyespot origins are not contingent on the presence ferred when both eyespots had a higher likelihood of be- of another eyespot on the wings may indicate that inde- ing present than absent in at least one shared ancestral pendent enhancers, or regulatory sequences, have node. Ancestral state likelihoods were calculated in Mes- evolved for each eyespot.

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