Our results suggest that signaling from the focus induces nested rings of regulatory gene expression that subsequently control the final color pattern. Furthermore, the remarkably plastic regulatory interactions downstream of focal signaling have facilitated the evolution of eyespot diversity.
Similar phenotypic changes have evolved independently in many animal taxa. It is unknown whether independent changes involve the same or different developmental and genetic mechanisms. Myriad pigment patterns in the genus Drosophila offer numerous opportunities to address this question. Previous studies identified regulatory and structural genes involved in the development and diversification of pigmentation in selected species. Here, we examine Drosophila americana and Drosophila novamexicana, interfertile species that have evolved dramatic pigmentation differences during the few million years since their divergence. Interspecific genetic analysis was used to investigate the contribution of five specific candidate genes and other genomic regions to phenotypic divergence by testing for associations between molecular markers and pigmentation. At least four distinct genomic regions contributed to pigmentation differences, one of which included the ebony gene. Ebony protein was expressed at higher levels in the more yellow D. novamexicana than the heavily melanized D. americana. Because Ebony promotes yellow pigment formation and suppresses melanization, the expression difference and genetic association suggest that evolution at the ebony locus contributed to pigmentation divergence between D. americana and D. novamexicana. Surprisingly, no genetic association with the yellow locus was detected in this study, and Yellow expression was identical in the two species. Evolution at the yellow locus underlies pigmentation divergence among other Drosophila species; thus, similar pigment patterns have evolved through regulatory changes in different genes in different lineages. These findings bear upon understanding classic models of melanism and mimicry. S imilar functional requirements or selective pressures have favored the independent evolution of similar structures or pattern elements in multiple lineages. The webbing of digits in aquatic or semiaquatic tetrapods, the wings of birds, bats, and pterosaurs, and wing color patterns in butterfly mimicry rings have evolved independently. One of the fundamental questions raised by these examples of convergent evolution is whether the genetic and developmental mechanisms underlying similar evolutionary changes are the same or different.The evolution of pigmentation offers an attractive model for analyzing phenotypic convergence, because similar phenotypes have arisen frequently in a wide variety of organisms. For example, melanic forms have evolved in nearly all animal taxa (1). In some bird and mammal species, amino acid changes in the melanocortin receptor protein, which activates melanin synthesis, have caused melanism in natural populations (ref. 2 and refs. therein). Although this finding suggests that melanism in some vertebrates shares a common genetic and developmental basis, it is not known whether this is also the case in other taxa, such as insects. Pigmentation in vertebrates and insects forms through different cellular mechanisms (3, 4), which may affect the gen...
. The morphological diversification of insect hindwings has involved the acquisition of different sets of target genes by Ubx in different lineages. Changes in Hox-regulated target gene sets are, in general, likely to underlie the morphological divergence of homologous structures between animals.
Background The diversity of butterfly color patterns can be attributed to a relatively small number of pattern elements that are homologous across Lepidoptera. Although genes involved in patterning some of these elements have been identified, the development of several major elements remains poorly understood. To identify genes underlying wing pupal cuticle markings and wing margin color patterns, we examined expression of the candidate transcription factors Engrailed/Invected (En/Inv), Distal-less (Dll), Cubitus interruptus (Ci), and Spalt in two nymphalids: Junonia coenia and Bicyclus anynana. Results We found that En/Inv, Dll, and Ci mark domains on the J. coenia last-instar forewing disc that closely correspond to the position and shape of pupal cuticle markings. We also found that Spalt demarcates wing margin color patterns in both J. coenia and B. anynana, and that CRISPR/Cas9 deletions in the spalt gene result in reduction and loss of wing margin color patterns in J. coenia. These data demonstrate a role for spalt in promoting wing margin color patterning, in addition to its previously described role in eyespot patterning. Conclusion Our observations support the model that a core set of regulatory genes are redeployed multiple times, and in multiple roles, during butterfly wing pattern development. Of these genes, spalt is of special interest as it plays a dual role in both eyespot and margin color pattern development.
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