14) Antonia Monteiro and the Origin for Nymphalid Butterfly Eyespots (by Rey J. Rosa Morales)

Dr. Antonia Monteiro (Assistant Professor in Yale University since 2006; see image 1). One of her interest is the study of the origins of wing butterflies eyespot (image 2). Based on the theory of co-option (or exaptation, read blog# 13 for more information), that explains that genes possibly shift in the function of a trait during evolution. For example, a trait can evolve because on a time can served for a particular function, but subsequently it may come to serve another function.

Image 1. At left side Omar Delannoy-Bruno, student in developmental biology field; (at center) Dr. Antonia Monteiro (main guest invited); (at right side) Rey J. Rosa Morales (author of this entry blog) in Old San Juan, Puerto Rico.

Image 2. Eyespot in butterfly wing

According to Monteiro and her group (2012) they discover that from both morphological and developmental perspectives of homology [1,3,4], nymphalid eyespots and an associated gene cluster arose a single time, early in the evolution of the Nymphalidae (see image 3). In addition, this single origin, multiple losses of gene expression have occurred, suggesting a novel means in which complex traits originate: from an initial gene regulatory network co-option followed by stream-lining of extraneous network elements. Moreover, they also found that the origin of eyespots was concurrent with the origin of the gene expression patterns, approximately 90 million years ago. This finding suggests that complex traits such as butterfly eyespots may initially evolve by re-deploying pre-existing gene regulatory networks, which are subsequently trimmed of genes that are unnecessary in the novel context.

Image 3. Nymphalidae subfamilies

In the study, they obtain the results from a morphological assessment of homology; they used Mayr’s definition where ‘‘a feature is homologous in two or more taxa if it can be traced back to the same feature in the presumptive common ancestor.’’ [2]. If eyespots are homologous, there should be a single origin of this trait; in contrast, multiple origins of eyespots within the Nymphalidae would demonstrate that the traits are not homologous [7]. (see Figure 1 and 2).

Figure 1. Origins of eyespots and associated gene expression. (A) Origin of eyespots inferred from 399 nymphalid and 29 outgroup species from phylogeny in reference 3. (B) Origin of expression in eyespot centers inferred from gene expression profiles of 23 species. Presence or absence of expression of genes in future eyespot centers indicated by black and white boxes, respectively, and grey boxes indicate species/gene combinations for which expression data are unavailable. Green bars indicate two independent origins of eyespot-associated Antp expression. In both (A) and (B), divergence times (in millions of years) are from reference 3, 7; red bars on the phylogeny indicate the possible locations of the single origin of eyespots, while gold bars indicate possible locations for the single origin of gene expression for sal, Notch, Dll, and possibly en in the eyespot centers. Asterisks (*) indicate species for which expression data are from [5,6].

Figure 2. Regulatory network simplification in a complex trait. Following the origin of a complex trait and its underlying developmental gene regulatory network, genes that are non-functional or unnecessary may be subsequently removed from the network (genes 2 and 3), without eliminating the trait. Genes expressed in homologous traits of all taxa may represent a ‘core network’ of regulatory elements (genes 1 and 4) that are necessary for the development of the novel trait.

References:

1. Abouheif A (1999) Establishing homology criteria for regulatory gene networks: prospects and challenges. In: Bock GR, Cardew G, editors. Homology. Novartis Foundation Symposium 222. Chichester: Wiley. pp. 207–225.
2. Mayr E (1982) The Growth of Biological Thought. Cambridge, MA: Harvard Univ Press. 
3. Monteiro, A. (2012). A Single Origin for Nymphalid Butterfly Eyespots Followed by Widespread Loss of Associated Gene Expression. PLOS Genetics 8(8):1-7.
4. Monteiro A (2012) Gene regulatory networks reused to build novel traits: Co- option of an eye-related gene regulatory network in eye-like organs and red wing patches on insect wings is suggested by optix expression. Bioessays 34: 181–186.
5. Saenko SV, Marialva MSP, Beldade P (2011) Involvement of the conserved Hox gene Antennapedia in the development and evolution of a novel trait. EvoDevo 2: 9.
6. Shirai LT, Saenko SV, Keller RA, Jeronimo MA, Brakefield PM, et al. (2012) Evolutionary history of the recruitment of conserved developmental genes in association to the formation and diversification of a novel trait BMC Evol Biol 12: 21.
7. Wake DB, Wake MH, Specht CD (2011) Homoplasy: from detecting pattern to determining process and mechanism of evolution. Science 331:1032–1035.