The Cellular Expression and Genetics of an Established Polymorphism in Poecilia 1167 Reticulata; “Purple Body, (Pb)” Is an Autosomal Dominant Gene, 1168 2

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The Cellular Expression and Genetics of an Established Polymorphism in Poecilia 1167 Reticulata; “Purple Body, (Pb)” Is an Autosomal Dominant Gene, 1168 2 bioRxiv preprint doi: https://doi.org/10.1101/121277; this version posted March 28, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 1 The Cellular Expression and Genetics of an 2 Established Polymorphism in Poecilia reticulata; 3 “Purple Body, (Pb)” is an Autosomal Dominant 4 Gene 5 Alan S. Bias1 and Richard D. Squire2 6 7 1Independent Researcher and Swordtail Guppy Breeder. Mailing address: P.O. Box 1508, 8 Lewisburg, West Virginia 24901, USA. orcid.org/0000-0002-9093-619X. [email protected] 9 10 2Biology Department (retired), University of Puerto Rico, Mayaguez campus, Mayaguez, 11 Puerto Rico, USA. Mailing address: P. O. Box 3227, Mayaguez, P.R., USA 00681-3227. 12 orcid.org/0000-0002-3916-0672. [email protected] 13 14 Abstract. Modification of wild-type carotenoid orange and pteridine red coloration and spotting of male ornaments 15 in both wild populations of Poecilia reticulata (Guppies) and modern Domestic Guppy strains by the Purple Body 16 gene has long been overlooked in research articles and little understood in breeder publications. This modification is 17 commonly found in wild-type Poecilia reticulata reticulata populations from numerous collection sites and has been 18 photographed but not recognized in these collections. It is non-existent or near absent in collections taken from 19 variant populations of Poecilia reticulata wingei. We identify and determine the mode of inheritance, cellular and 20 phenotypic expression by the Purple gene in these stocks. The Purple Body color pigment modification is a distinct 21 polymorphism in wild P. reticulata reticulata populations. Its existence suggests multiple benefits that satisfy female 22 sexual selection preferences, and minimize or reduce potential predation risks. Photographic and microscopic 23 evidence demonstrated that Purple Body is a normal polymorphism in wild and domestic guppies modifying color 24 pigment regions. Purple Body is inherited as an autosomal incompletely dominant trait. 25 Key Words: Guppy color and modifications, chromatophore, violet iridophore, blue iridophore, violet- 26 blue iridophore, xanthophore, xantho-erythrophore, Purple Guppy, Purple Body gene, Metal Gold 27 Iridophore, Poecilia reticulata, Poecilia obscura, Poecilia wingei, Cumana’ Guppy, Campoma Guppy, 28 Endler’s Livebearer. 29 30 31 Fig 1. Wild-type Purple Body (Pb) males in heterozygous condition. 32 1 bioRxiv preprint doi: https://doi.org/10.1101/121277; this version posted March 28, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 33 Introduction 34 The intent of this paper is multifold; 1. Identify the mode of inheritance of the Purple 35 Body trait. 2. Provide photographic and microscopic exhibits of Purple Body and non-Purple 36 Body for ease in identification. 3. To encourage future study interest at a cellular level of 37 populations in which Purple Body highlights near-UV (Ultra-Violet) reflective qualities. 4. 38 To stimulate molecular level studies of Purple Body and to identify the linkage group (LG) to 39 which it belongs. 40 A generally accepted definition of polymorphism states: “(1) Polymorphism is the 41 occurrence together in the same habitat of two or more distinct forms of a species in such 42 proportions that the rarest of them cannot be maintained by recurrent mutation. (2) If a 43 genetically controlled form occurs in even a few percent of a population it must have been 44 favored by selection. (3) Polymorphism may either be transient, in which a gene is in 45 process of spreading through a population unopposed, or balanced, in which it is maintained 46 at a fixed level by a balance of selective agencies. (4) Owing to the recurrent nature of 47 mutation, transient polymorphism is generally due to changes in the environment, which 48 make the effects of a previously disadvantageous gene beneficial (Ford 1945).” 49 Wild Poecilia reticulata, both in native populations and feral introductions, exist in a 50 previously undocumented polymorphic state; Purple Body and non-Purple Body. In 51 Domestic strains both polymorphisms persist as a direct result of intended breeder 52 intervention and as an unintended result of outcrosses between fixed phenotypic strains. 53 Therefore, it is safe to assume that the co-existence of two sympatric phenotypes, in both 54 wild and domestic stocks, must confer a selective advantage. The two most likely 55 possibilities are reduction in predation and/or favoritism in sexual selection. 56 For nearly 100 years published research has focused on “heritability, brightness, 57 intensity of orange chroma and hue in male ornaments (Winge 1922a, 1927; Lindholm 58 2002; Deere 2012), most often in the context of sexual selective preference or 59 environmental carotenoid intake. Over the last decades we have seen a gradual shift 60 towards identification of benefits derived from the reflective qualities of iridophore biased 61 phenotypes. This frequently involved the study of Opsin, and UV and near-UV spectrum 62 vision in Guppies and their predators. Additional consideration was given to the nature of 63 ornaments being composite traits with independent origins (Grether 2004). 64 P. reticulata pteridine based color appears as shades of red, while carotenoid color is 65 more yellow-orange. The "wild-type" guppy red is maintained in a variety of environments 66 by synthesizing sufficient pteridines to balance the amount of dietary carotenoids obtained 67 from food sources. Iridophore development begins in embryonic stages, continues with 68 onset of sexual maturity and is completed in young adulthood. Reflective qualities of 69 iridophores increase with maturation and development of guanine crystals (Gundersen 70 1982; Deere 2012). Intensity and reflective qualities of coloration are complemented by 71 both underlying basal and ectopic melanophores. 72 Studies on extreme polymorphic variation found within Poeciliid species over the last 73 100 years abound involving P. reticulata, P. parae, P. picta. For the most part those within 74 wild Poecilia reticulata and Poecilia reticulata wingei have focused on “wild-type” orange 75 color pigmentation of spotting; its benefits from carotenoid intake, Y-linked inheritance for 76 spotting, female sexual selection preferences, and heterogametic benefits in the form of 77 reduced predation on females. Of late emphasis has seen a shift towards benefits derived 78 from both UV and near-UV coloration. 79 Xantho-erythrophores primarily utilize the absorbed carotenoids ingested from local 80 dietary resources. Carotenoid availability produces variability in expression within and 81 between populations (Grether 1999). This is in contrast to red drosopterin based color 82 pigment, which is synthesized by the individual de novo (Goodwin 1986). Male orange 83 ornaments are the product of both orange carotenoids and red pteridine color pigments: 84 drosopterins. 2 bioRxiv preprint doi: https://doi.org/10.1101/121277; this version posted March 28, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 85 A direct correlation between carotenoid intake and higher levels of drosopterin synthesis 86 has been identified. While pteridine red and tunaxanthin carotenoid orange were identified 87 in male spotting, only the carotenoid orange was obtained from the algae in the 88 environment in wild study populations (Grether 2001). Counter-gradient variability found in 89 male orange ornaments from multiple locales has been documented (Grether 2005a, 90 2005b; Deere 2012) as the result genetic differences between populations. The ratio of 91 carotenoids and drosopterins had a direct effect on size and hue of orange spotting. 92 Research utilizing Domestic Guppies has proven both X and Y-linked inheritance for red 93 color pigmentation in finnage (Khoo and Phang 1999). Documented results by Domestic 94 Guppy Breeders reveal many strains have been produced with both X and Y-linked 95 inheritance for red color pigment in both body and finnage. Many females capable of 96 passing red in domestic Guppy stocks often express coloration, while others resembling wild 97 color / tail neutral guppy females do not. 98 Wild-type female guppies in native locales, and domestic strains, lacking coloration are 99 also capable of passing on unexpressed red color pigment to daughters and expressed color 100 pigment to sons (Gordon 2012; Bias, unpublished breeding results). Such sexual 101 dimorphism reduces predation on females, while allowing it to varying extents on males. 102 Continued breeding’s in Domestic strains are now showing that red color pigment is not 103 simply the result of an XY-linked mode of inheritance, but are also suggestive of autosomal 104 linkage as well. A recent publication involving red color morphs found within Poecilia picta 105 supports this assertion (Lindholm 2015). 106 The purple phenotype has been present in hobbyist stocks for decades, but has been 107 largely unrecognized except in the case of pure-bred all-purple strains, such
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