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Abdominal pigmentation in Drosophila melanogaster

Abdominal pigmentation in Drosophila melanogaster is a morphologically simple but highly variable trait that often has adaptive significance.  Pigmentation has extensively been studied in Drosophila melanogaster.  It has been used as a model for understanding the development and evolution of morphological phenotypes.[1]

Pigmentation shows enormous phenotypic variation between species, populations, and individuals, and even within individuals during ontogeny.[2][3][4][5][6][7] It gives rise to natural variation, polyphenism and sexual dimorphism.[8][9][10] It also varies between species, contributing to species recognition, mate choice, thermoregulation, protection (warning signals), mimicry, and crypsis.[11][12][13] Changes in pigmentation are often adaptive and vital to the fitness of the organism.[11] Much is known about the genes that regulate the biochemical synthesis of pigments in D. melanogaster and the genes that control the temporal and spatial distribution of this biosynthesis.[9]

Not only is body pigmentation ecologically relevant in Drosophila but it is also a relatively simple and easily measured phenotype to study the genetic architecture of natural variation in complex traits.[9][13] Each tergite of female D. melanogaster generally has a stripe of dark coloration (melanin) on a lighter tan background (sclerotin). During pre-and post-ecdysis, the epidermal cells underlying the cuticle secrete tyrosine-derived catecholamines into the cuticle for sclerotinization and melanisation.[13][14]

The melanin/sclerotin biosynthetic pathway and its underlying genetic basis have been well studied. However, many of the genes known to affect D. melanogaster pigmentation do not form part of this pathway or any parallel pathway.[15] Furthermore, the genes that lead to natural variation in body pigmentation are not necessarily the same genes that are directly involved in the biosynthesis of melanin and sclerotin. By mapping the genetic basis of natural variation in body pigmentation, new genes affecting pigment biosynthesis as well as regulatory regions that determine when and where pigmentation will develop were discovered.[10][16]

The yellow gene

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The yellow gene is required for the production of black melanin and in the absence of yellow, black melanin is replaced by brown melanin. In Drosophila melanogaster, yellow is sex-specifically regulated in the posterior abdomen. Furthermore, the evolution of wing or abdominal pigmentation patterns between Drosophila species correlates with modifications of yellow spatial expression.[17][18][19][11] Temperature also controls the spatial expression of yellow in the abdominal epidermis of pharate females.

By contrast, yellow expression associated with bristles is not modulated by temperature. yellow is known to be required but not sufficient for black melanin production.[17] Studies have indicated that the black melanin is Dopamine-melanin and not Dopa-melanin. The combined over-expression of yellow and tan at 29 °C is necessary and sufficient to reproduce the black phenotype observed at 18°C. Thus, the stronger expression of yellow at 18°C also contributes to thermal plasticity of female abdominal pigmentation.

yellow is required but not sufficient for production of black pigment. Indeed, yellow gain- of-function must be combined to ebony down-regulation or tan up-regulation to induce a fully black pigmentation.[11] In order to test whether the strong expression of yellow and tan is sufficient to explain the black pigmentation observed at 18 °C, the researcher increased their expression in abdominal epidermis at 29 °C to mimic the effect of lower temperature.

On comparing the cuticles of wild-type females and females over-expressing either yellow (pnr-Gal4/UAS-y), tan (UAS-t/+; pnr-Gal4/+) or both yellow and tan (UAS-t/+; UAS-y/pnr-Gal4) at 29 °C. The yellow over-expression does not change pigmentation whereas tan over-expression induces dark pigmentation in the anterior region of the tergites.[17][20] However, careful examination revealed that this ectopic pigmentation was not as dark as the normal pigmentation in the posterior region of the tergites. This was more visible in A4 and A5 segments. By contrast, when both yellow and tan were over-expressed in the dorsal region of the abdomen, the anterior region of the tergites was as black as the posterior border of the tergites. This shows that yellow and tan combined over-expression at 29 °C is necessary and sufficient to reproduce the pigmentation phenotype observed at low temperature.

Production of dopamine-melanin by the yellow gene

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Yellow gene is required for the production of Dopamine-melanin. Yellow is related to two other enzymes, Yellow-f and Yellow-f2, which can be used as substrate for Dopachrome with a higher efficiency than Dopamine-chrome. Some authors have proposed that the black pigment in abdominal cuticle was Dopa-melanin produced from Dopa.[11][20] Incubation of abdominal cuticles or wings of unpigmented pharates with Dopamine is sufficient to produce black pigment, which suggests that this black pigment is produced from Dopamine and is therefore Dopamine-melanin.[21][22] It is also known that Ddc down-regulation leads to a complete loss of black and brown pigments.

Effect of temperature

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Abdominal pigmentation in Drosophilids represents an appropriate model to dissect the molecular bases of phenotypic plasticity as it is sensitive to temperature in many species.[23] Abdominal pigmentation of Drosophila melanogaster females is darker when they develop at low temperature. This is particularly pronounced in posterior abdominal segment. Plasticity of abdominal pigmentation is likely to have functional consequences as abdominal pigmentation has been linked to thermoregulation and resistance to UV, pathogens or parasites.[24] Abdominal pigmentation is also associated to resistance to desiccation.[25]

Abdominal pigmentation differs between males and females in several Drosophila species and has been used as a model to dissect the genetic bases of sexual dimorphism.[26][10] Furthermore, as abdominal pigmentation is highly evolvable, it has been investigated to study the molecular bases of morphological variation within species.[27] The genes involved in Drosophila abdominal pigmentation are relatively well known, in particular those encoding the enzymes required for the synthesis of cuticle pigments.[28][29][22] It has been reported recently that the thermal plasticity of female abdominal pigmentation in Drosophila melanogaster involves transcriptional modulation of the pigmentation gene tan (t).[11] This gene encodes a hydrolase implicated in the production of melanin.[17] tan is seven times more expressed at 18 °C than at 29 °C in the posterior abdominal epidermis of young adult females.

Temperature modulation

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It is shown by RT-qPCR that yellow expression is modulated by temperature in the epidermis of abdominal segments A5, A6 and A7 in female pharates (1.97 fold more expressed at 18 °C than at 29 °C).[22] In order to analyse the spatial expression of y, many researchers performed in-situ hybridization of female pharates grown at 18 °C or 29 °C and could distinguish three stages of yellow expression (A, B and C) based on the degree of maturation of abdominal bristles . These stages correspond approximately to a transition from stage P11(i) to stage P12(ii) as described by Bainbridge and Bownes with morphological markers at 25 °C.[30]

In stage A pharates, two cells at the base of bristles expressed y. This expression had a similar intensity when pharates were raised at 18 °C and at 29 °C. These two cells are likely to be the socket and the shaft, the only pigmented cells of the bristle organ. In addition, yellow was expressed in the posterior region of each tergite in segments A2 to A6. This expression was much broader and stronger in pharates grown at 18 °C compared to 29 °C. In A6, yellow was expressed in the whole tergite at 18 °C, and only in the posterior region of the tergite at 29 °C. In A7, at 18 °C, the whole tergite expressed yellow at a high level, whereas it was much weaker at 29 °C.

In stage B pharates, yellow expression was reduced in the socket and the shaft, while the bristle began to be pigmented. Furthermore, yellow was still more expressed in the abdominal epidermis of pharates grown at 18 °C than at 29 °C.

In stage C pharates, yellow was no longer expressed at the base of bristles and the bristles were almost fully pigmented. Furthermore, its overall expression in tergites was reduced compared to stage B and more similar between pharates grown at 18 °C and 29 °C.[30]

Regulation of pigmentation

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Hox genes have been implicated in the evolution of many animal body patterns. Hox protein directly activates expression of the yellow pigmentation gene in posterior segments. In D. melanogaster, the male has fully pigmented tergites in the fifth and sixth abdominal segments (A5 and A6), whereas the female's tergites have only a narrow pigment stripe. This sexually dimorphic pigmentation pattern is controlled by a genetic regulatory circuit involving the Hox gene Abd-B. Loss-of-function mutations of Abd-B cause the loss of male-specific pigmentation, while gain-of-function alleles, such as Abd-BMcp, cause the expansion of pigmentation to the A4 segment or even to the thorax. The sexually dimorphic pigment pattern depends upon regulatory interactions among the Abd-B, bab, and dsx genes.[26]

Pigmentation of the posterior male abdomen is a trait found in many members of the melanogaster species group but not in several other major groups. The dimorphic regulation of bab expression is closely correlated with dimorphic pigmentation as well other pigmentation patterns. It is not known, however, which regulatory interactions among Abd-B, bab, dsx, and pigmentation genes are direct and which are indirect.[31]

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ectopic pigmentation

References

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  1. ^ Saleh Ziabari O, Shingleton AW (June 2017). "Quantifying Abdominal Pigmentation in Drosophila melanogaster". Journal of Visualized Experiments (124): 55732. doi:10.3791/55732. PMC 5608185. PMID 28605370.
  2. ^ Wittkopp PJ, Beldade P (February 2009). "Development and evolution of insect pigmentation: genetic mechanisms and the potential consequences of pleiotropy". Seminars in Cell & Developmental Biology. 20 (1): 65–71. doi:10.1016/j.semcdb.2008.10.002. hdl:10400.7/197. PMID 18977308.
  3. ^ Lindgren J, Moyer A, Schweitzer MH, Sjövall P, Uvdal P, Nilsson DE, et al. (August 2015). "Interpreting melanin-based coloration through deep time: a critical review". Proceedings. Biological Sciences. 282 (1813): 20150614. doi:10.1098/rspb.2015.0614. PMC 4632609. PMID 26290071.
  4. ^ Kronforst MR, Papa R (May 2015). "The functional basis of wing patterning in Heliconius butterflies: the molecules behind mimicry". Genetics. 200 (1): 1–19. doi:10.1534/genetics.114.172387. PMC 4423356. PMID 25953905.
  5. ^ Albert NW, Davies KM, Schwinn KE (2014-06-13). "Gene regulation networks generate diverse pigmentation patterns in plants". Plant Signaling & Behavior. 9 (9): e29526. Bibcode:2014PlSiB...9E9526A. doi:10.4161/psb.29526. PMC 4205132. PMID 25763693.
  6. ^ Monteiro A (January 2015). "Origin, development, and evolution of butterfly eyespots". Annual Review of Entomology. 60 (1): 253–71. doi:10.1146/annurev-ento-010814-020942. PMID 25341098.
  7. ^ Kronforst MR, Barsh GS, Kopp A, Mallet J, Monteiro A, Mullen SP, et al. (July 2012). "Unraveling the thread of nature's tapestry: the genetics of diversity and convergence in animal pigmentation". Pigment Cell & Melanoma Research. 25 (4): 411–33. doi:10.1111/j.1755-148x.2012.01014.x. PMID 22578174.
  8. ^ Lande R (March 1980). "Sexual Dimorphism, Sexual Selection, and Adaptation in Polygenic Characters". Evolution. 34 (2): 292–305. doi:10.2307/2407393. ISSN 0014-3820. JSTOR 2407393. PMID 28563426.
  9. ^ a b c Kopp A (June 2006). "Basal relationships in the Drosophila melanogaster species group". Molecular Phylogenetics and Evolution. 39 (3): 787–98. Bibcode:2006MolPE..39..787K. doi:10.1016/j.ympev.2006.01.029. PMID 16527496.
  10. ^ a b c Williams TM, Selegue JE, Werner T, Gompel N, Kopp A, Carroll SB (August 2008). "The regulation and evolution of a genetic switch controlling sexually dimorphic traits in Drosophila". Cell. 134 (4): 610–23. doi:10.1016/j.cell.2008.06.052. PMC 2597198. PMID 18724934.
  11. ^ a b c d e f Wittkopp PJ, Carroll SB, Kopp A (September 2003). "Evolution in black and white: genetic control of pigment patterns in Drosophila". Trends in Genetics. 19 (9): 495–504. doi:10.1016/s0168-9525(03)00194-x. PMID 12957543.
  12. ^ Llopart A, Elwyn S, Lachaise D, Coyne JA (November 2002). "Genetics of a difference in pigmentation between Drosophila yakuba and Drosophila santomea". Evolution; International Journal of Organic Evolution. 56 (11): 2262–77. doi:10.1111/j.0014-3820.2002.tb00150.x. PMID 12487356. S2CID 221733289.
  13. ^ a b c Andersen SO (March 2010). "Insect cuticular sclerotization: a review". Insect Biochemistry and Molecular Biology. 40 (3): 166–78. Bibcode:2010IBMB...40..166A. doi:10.1016/j.ibmb.2009.10.007. PMID 19932179.
  14. ^ Moussian B (May 2010). "Recent advances in understanding mechanisms of insect cuticle differentiation". Insect Biochemistry and Molecular Biology. 40 (5): 363–75. Bibcode:2010IBMB...40..363M. doi:10.1016/j.ibmb.2010.03.003. PMID 20347980.
  15. ^ True JR (December 2003). "Insect melanism: the molecules matter". Trends in Ecology & Evolution. 18 (12): 640–647. doi:10.1016/j.tree.2003.09.006.
  16. ^ Wright TR (1987). "The Genetics of Biogenic Amine Metabolism, Sclerotization, and Melanization in Drosophila Melanogaster". Molecular Genetics of Development. Advances in Genetics. Vol. 24. Elsevier. pp. 127–222. doi:10.1016/S0065-2660(08)60008-5. ISBN 978-0-12-017624-3. PMID 3124532.
  17. ^ a b c d Wittkopp PJ, Vaccaro K, Carroll SB (September 2002). "Evolution of yellow gene regulation and pigmentation in Drosophila". Current Biology. 12 (18): 1547–56. Bibcode:2002CBio...12.1547W. doi:10.1016/s0960-9822(02)01113-2. PMID 12372246. S2CID 2301246.
  18. ^ Gompel N, Prud'homme B, Wittkopp PJ, Kassner VA, Carroll SB (February 2005). "Chance caught on the wing: cis-regulatory evolution and the origin of pigment patterns in Drosophila". Nature. 433 (7025): 481–7. Bibcode:2005Natur.433..481G. doi:10.1038/nature03235. PMID 15690032. S2CID 16422483.
  19. ^ Ordway AJ, Hancuch KN, Johnson W, Wiliams TM, Rebeiz M (August 2014). "The expansion of body coloration involves coordinated evolution in cis and trans within the pigmentation regulatory network of Drosophila prostipennis". Developmental Biology. 392 (2): 431–40. doi:10.1016/j.ydbio.2014.05.023. PMID 24907418.
  20. ^ a b Wittkopp PJ, Stewart EE, Arnold LL, Neidert AH, Haerum BK, Thompson EM, et al. (October 2009). "Intraspecific polymorphism to interspecific divergence: genetics of pigmentation in Drosophila". Science. 326 (5952): 540–4. Bibcode:2009Sci...326..540W. doi:10.1126/science.1176980. PMID 19900891. S2CID 6796236.
  21. ^ Jeong S, Rebeiz M, Andolfatto P, Werner T, True J, Carroll SB (March 2008). "The evolution of gene regulation underlies a morphological difference between two Drosophila sister species". Cell. 132 (5): 783–93. doi:10.1016/j.cell.2008.01.014. PMID 18329365. S2CID 15447569.
  22. ^ a b c Walter MF, Zeineh LL, Black BC, McIvor WE, Wright TR, Biessmann H (1996). "Catecholamine metabolism and in vitro induction of premature cuticle melanization in wild type and pigmentation mutants of Drosophila melanogaster". Archives of Insect Biochemistry and Physiology. 31 (2): 219–33. doi:10.1002/(sici)1520-6327(1996)31:2<219::aid-arch9>3.0.co;2-u. PMID 8580497.
  23. ^ Ramniwas S, Kajla B, Dev K, Parkash R (April 2013). "Direct and correlated responses to laboratory selection for body melanisation in Drosophila melanogaster: support for the melanisation-desiccation resistance hypothesis". The Journal of Experimental Biology. 216 (Pt 7): 1244–54. doi:10.1242/jeb.076166. PMID 23239892. S2CID 22483971.
  24. ^ Kutch IC, Sevgili H, Wittman T, Fedorka KM (October 2014). "Thermoregulatory strategy may shape immune investment in Drosophila melanogaster". The Journal of Experimental Biology. 217 (Pt 20): 3664–9. doi:10.1242/jeb.106294. PMID 25147243. S2CID 6798309.
  25. ^ Rajpurohit S, Peterson LM, Orr AJ, Marlon AJ, Gibbs AG (2016-09-22). "An Experimental Evolution Test of the Relationship between Melanism and Desiccation Survival in Insects". PLOS ONE. 11 (9): e0163414. Bibcode:2016PLoSO..1163414R. doi:10.1371/journal.pone.0163414. PMC 5033579. PMID 27658246.
  26. ^ a b Kopp A, Duncan I, Godt D, Carroll SB (November 2000). "Genetic control and evolution of sexually dimorphic characters in Drosophila". Nature. 408 (6812): 553–9. Bibcode:2000Natur.408..553K. doi:10.1038/35046017. PMID 11117736. S2CID 261526.
  27. ^ Riedel F, Vorkel D, Eaton S (January 2011). "Megalin-dependent yellow endocytosis restricts melanization in the Drosophila cuticle". Development. 138 (1): 149–58. doi:10.1242/dev.056309. PMID 21138977. S2CID 29017593.
  28. ^ Massey JH, Wittkopp PJ (2016). "The Genetic Basis of Pigmentation Differences within and Between Drosophila Species". Genes and Evolution. Current Topics in Developmental Biology. Vol. 119. Elsevier. pp. 27–61. doi:10.1016/bs.ctdb.2016.03.004. ISBN 978-0-12-417194-7. PMC 5002358. PMID 27282023.
  29. ^ Gibert JM, Mouchel-Vielh E, De Castro S, Peronnet F (August 2016). "Phenotypic Plasticity through Transcriptional Regulation of the Evolutionary Hotspot Gene tan in Drosophila melanogaster". PLOS Genetics. 12 (8): e1006218. doi:10.1371/journal.pgen.1006218. PMC 4980059. PMID 27508387.
  30. ^ a b Bainbridge SP, Bownes M (January 1988). "Ecdysteroid titers during Drosophila metamorphosis". Insect Biochemistry. 18 (2): 185–197. doi:10.1016/0020-1790(88)90023-6. ISSN 0020-1790.
  31. ^ Gompel N, Carroll SB (August 2003). "Genetic mechanisms and constraints governing the evolution of correlated traits in drosophilid flies". Nature. 424 (6951): 931–5. Bibcode:2003Natur.424..931G. doi:10.1038/nature01787. PMID 12931186. S2CID 4415001.
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