Drosophilapigmentation evolution: Divergent genotypes underlying convergent phenotypes

Abstract

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...

Development and evolution of insect pigmentation: Genetic mechanisms and the potential consequences of pleiotropy

“…For three of these four genes (bric-a-brac [7], yellow [4], and tan [5]), functional cis-regulatory changes have been identified, with changes in bric-a-brac and yellow shown to alter binding sites for highly pleiotropic transcriptional regulators (Doublesex [7], Abdominal-B [5,7], and Engrailed [4]). For ebony, cis-regulatory changes have not been definitively proven, but data are consistent with cis-regulatory divergence [26].…”

“…Within D. melanogaster, genetic mapping suggests that functional variants affecting pigmentation lie within both transcriptional regulators (bric-a-brac [23], optomotor-blind [24]) and pigment synthesis genes (ebony [25]). Between Drosophila species, genetic mapping suggests functional divergence at loci encoding pigment synthesis effector genes (ebony [26], tan [5,27]), although these studies do not exclude a role for patterning genes. Both patterning (bric-a-brac [28]) and effector (yellow [29], ebony [26], tan [5]) genes have expression differences that correlate with pigmentation divergence between species.…”

“…Between Drosophila species, genetic mapping suggests functional divergence at loci encoding pigment synthesis effector genes (ebony [26], tan [5,27]), although these studies do not exclude a role for patterning genes. Both patterning (bric-a-brac [28]) and effector (yellow [29], ebony [26], tan [5]) genes have expression differences that correlate with pigmentation divergence between species. For three of these four genes (bric-a-brac [7], yellow [4], and tan [5]), functional cis-regulatory changes have been identified, with changes in bric-a-brac and yellow shown to alter binding sites for highly pleiotropic transcriptional regulators (Doublesex [7], Abdominal-B [5,7], and Engrailed [4]).…”

Genetic mechanisms and constraints governing the evolution of correlated traits in drosophilid flies

“…We infer that Bab2 does not repress pigmentation in this species, which allows dark pigmentation of A6 in the female. The expanded posterior pigmentation in D. serrata females is a convergent pattern that must have evolved through a different genetic pathway, independent of bab, indicating that phenotypic convergence does not necessarily rely on the same genetic mechanism 1,13 . We suggest that control of the trichome pattern by bab2 has been maintained in D. melanogaster, Figure 2 Modulation of Bab2 expression underlies the diversification and evolutionary convergence of cuticular traits throughout the Drosophilinae.…”

Extrapolating from local ecological processes to genus-wide patterns in colour polymorphism in South AfricanProtea

“…Although these assumptions are strengthened by parallels with ecological speciation [74], they ignore the genetic mechanisms underlying colour polymorphism, which may differ among species and constrain certain evolutionary outcomes. Different mutations can produce the same or similar pigment patterns in congeneric and even conspecific plants or animals, but each mutation may nevertheless have its own set of pleiotropic effects [29,75,76]. In plants, mutations that halt anthocyanin production may occur in structural genes for the flavonoid biochemical pathway or in transcription factor regions, with the latter presumed more tissue-specific and the former more deleterious for their plant-wide effects on the pathway by-products, including compounds that reduce physiological stress or herbivory [29].…”