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Revista Brasileira de Ornitologia 26(4): 251–257. ARTICLE December 2018 Plumage polymorphism and variation in the melanocortin-1 receptor gene in the Fuscous Flycatcher, Cnemotriccus fuscatus (Wied, 1831) 1 1 2 1,3 Sandriéllem Natália Vieira , Juliana Araripe , Alexandre Aleixo & Péricles Sena do Rêgo Laboratório de Genética e Conservação, Instituto de Estudos Costeiros, Universidade Federal do Pará, 68600-000, Bragança, PA, Brazil. Coordenação de Zoologia, Museu Paraense Emílio Goeldi, Belém, PA, Brazil. Corresponding author: email@example.com Received on 26 October 2017. Accepted on 03 December 2018. ABSTRACT: We investigated the possible mechanisms behind the variation plumage color of the Fuscous Flycatcher, Cnemotriccus fuscatus, by sequencing the melanocortin-1 receptor (MC1R) gene, which has been associated with the variation in plumage coloration in birds. C. fuscatus is widely distributed in South America and includes seven subspecies, which diff er in their plumage coloration. Here we tested the hypothesis that the variation in the MC1R gene explains the plumage polymorphism found in C. fuscatus. We sequenced the MC1R gene in six subspecies, representing two groups: group 1 (yellow morph), with three subspecies, C. f. duidae, C. f. fumosus, and C. f. fuscatus, and group 2 (white morph), with the remaining subspecies, C. f. bimaculatus, C. f. beniensis, and C. f. fuscatior. Th e only variation we found among the C. fuscatus sequences were six non-synonymous substitutions from 22 variable sites, none of which were associated systematically with either plumage morph. Th e result of the neutrality test indicated that the polymorphism of the MC1R gene is not suggestive of signifi cant selection pressure. We conclude that variation in plumage coloration in C. fuscatus does not appear to be determined by the MC1R gene, and that it may be related to other loci or under the infl uence of environmental factors. KEY-WORDS: birds, MC1R gene, mutation, pigmentation, Tyrannidae. INTRODUCTION the diff erentiation of the plumage in avian species, due to the association between mutations in this gene and Th e variation in plumage coloration has been studied the phenotypic variation found in a number of diff erent from ecological, evolutionary and genetic perspectives groups of wild birds (Johnson et al. 2012, Ran et al. 2016). For example, single non-synonymous mutations (Hoekstra & Price 2004, Mundy 2005, Uy et al. 2016). Such diversity has been related to visual communication, in the MC1R gene were associated with plumage and may have evolved in response to the evolution of polymorphisms in the bananaquit (Coereba fl aveola) and the avian visual system (Osorio & Vorobyev 2008), the chestnut-bellied monarch, Monarcha castaneiventris although there is also some evidence that changes (Th eron et al. 2001, Uy et al. 2009). Studies in birds have also shown that the MC1R gene controls the amount of in plumage coloration may be a response to varying pressures in diff erent types of habitat (Gomez & Th éry both eumelanin (brown/black) and pheomelanin (red/ 2004, McNaught & Owens 2002). Many questions yellow) produced (Takeuchi et al. 1996, Wen et al. 2015). remain unresolved, however, on the evolution of In particular, García-Borrón et al. (2005) showed that the plumage coloration and its relation to speciation in birds yellow (pheomelanin) phenotype is produced by recessive MC1R extension (e) alleles. (Stoddard & Prum 2011, Seddon et al. 2013), such as the mechanisms that mediate the change in coloration In this context, we investigated the variation in between juveniles and adults (Galván & Jorge 2015), and coloration found among the subspecies of the Fuscous the factors determining changes in coloration despite the Flycatcher, Cnemotriccus fuscatus, a monotypic genus considerable energetic costs of this process (Legagneux et widely distributed in South America (Fig. 1). Th ere are seven C. fuscatus subspecies, which are diff erentiated not al. 2012, Mercadante & Hill 2014). Previous studies (e.g., Robbins et al. 1993, Vidal et only on the basis of their morphological characters, but al. 2010, Johnson et al. 2012) have suggested that the also their vocalizations and ecology (Fitzpatrick et al. melanocortin-1 receptor (MC1R) gene may be involved in 2004). Th ese subspecies can be divided into two groups, Plumage polymorphism in Fuscous Flycatcher, Cnemotriccus fuscatus Vieira et al. based primarily on the coloration of the belly, which is Belém, and the National Museum (MNRJ) in Rio de either white or yellow. Th ese fl ycatchers can be found in Janeiro. We followed the classifi cation of Fitzpatrick et al. a variety of habitats, including fl uvial islands, rainforest, (2004) to allocate the subspecies to two groups (yellow and dry forests, riparian habitats, and lowland and secondary white morphs). Group 1 (yellow morph) was composed forests (Rasmussen & Collar 2002). It is thus important of Cnemotriccus fuscatus duidae (n = 5 specimens), to understand which factors may infl uence the variation Cnemotriccus fuscatus fumosus (n = 7), and Cnemotriccus in the coloration of plumage found among the diff erent fuscatus fuscatus (n = 5), which are ventrally yellow to light subspecies of the Fuscous Flycatcher (Farnsworth & yellow. Group 2 (white morph) contained the other three Lebbin 2017). In particular, if a relationship can be found subspecies, Cnemotriccus fuscatus bimaculatus (n = 5), between genotype and phenotype, it might represent Cnemotriccus fuscatus beniensis (n = 3), and Cnemotriccus evidence of the role of natural selection in the fi xation of fuscatus fuscatior (n = 2), which are ventrally white or light subspecifi c coloration patterns (Hewitt 1988, Chunco et gray. Both male and female specimens were included, as al. 2007). C. fuscatus is not dichromatic (Fitzpatrick et al. 2004). Here we investigated the possible mechanisms Total DNA was isolated from the muscle tissue using that determine diff erentiation in plumage amongst the the Wizard Genomic DNA purifi cation kit (Promega), subspecies of C. fuscatus. Specifi cally, we tested whether following the manufacturer's instructions. To obtain a non-synonymous mutations in the sequence of the partial sequence of the MC1R gene, we amplifi ed the melanocortin-1 receptor (MC1R) gene were associated samples by PCR using the primers described by Cheviron systematically with variation in plumage coloration et al. (2006): lcorMSHR9 (5' – CTG GCT CCG GAA amongst the six subspecies, and whether these mutations GGC RTA GAT – 3') and lcorMSHR72 (5' – AYG CCA are suff ering selection pressures. GYG AGG GCA ACC A – 3'). Th e PCR conditions were the same as those used by Cheviron et al. (2006), and the PCR products were sequenced by Sanger's METHODS didesoxiterminal method (Sanger et al. 1977), using an ABI 3500 automatic sequencer. We sequenced 27 samples of Cnemotriccus fuscatus muscle Th e DNA sequences were aligned and their tissue (Table 1), representing six of the seven described nucleotides were compared to those from the bananaquit, subspecies. Th e samples were provided by the Goeldi Coereba fl aveola (GenBank access numbers AF362598 and Museum (MPEG: Museu Paraense Emilio Goeldi) in AF362601) and Gallus gallus (AB201631) using Bioedit Species distribution C. f. duidae C. f. fuscatus C. f. fumosos C. f. bimaculatus C. f. fuscatior C. f. beniensis Figure 1. Map showing the distribution of samples of Cnemotriccus fuscatus sequenced in this study. Yellow points represent specimens with yellow bellies and white points denote specimens with white bellies. Revista Brasileira de Ornitologia 26(4): 2018 Plumage polymorphism in Fuscous Flycatcher, Cnemotriccus fuscatus Vieira et al. Table 1. Location, coordinates, subspecies, voucher number, identifi cation code, and source of tissue used in this study. Locations Identifi cation of Subspecies Voucher number Institutions (Coordinates) the tissue Óbidos - PA Cfu1410, o * (00 37'50''N; C. f. fumosus CN1410, CN1378, MPEG Cfu1378 55 43'40''W) Chaves - PA 00 12'29.2''S; C. f. fumosus MARJ117, MARJ118 Cfu118, Cfu117 MPEG 49 58'39.2''W Marajó - PA (00 59'21''S; C. f. fumosus MAYA008 Cfu008 MPEG 49 56'24''W) Oriximiná - PA (1 45'36.89''S; C. f. fumosus ORX336, ORX359 Cfu336, Cfu359 MPEG 55 51'30.28''W) Porto Walter - AC (08 20'35.7''S; C. f. duidae UFAC1021 Cfu1021 MPEG 72 36'19.7''W) Japurá - AM JAP225, JAP267, JAP270 Cfu225, Cfu267, (02 02'31.5''S; C. f. duidae MPEG Cfu270 67 17'16.6''W) Porto Walter - AC (08 20'35.7''S; C. f. duidae UFAC0976 Cfu0976 MPEG 72 36'19.7''W) Uruçuí - PI (07 14'2.00''S; C.f. bimaculatus URC171 Cfu171 MPEG 44 33'1.55''W) Curimatá - PI (09 41'284''S; C.f. bimaculatus SRV005 Cfu005 MPEG 44 14'200''W) Redenção do Gurgueia - PA (9 38'022''S; C.f. bimaculatus SRV042 CfuS042 MPEG 44 08'807''W) Borba, Puruzinho, Ilha - AM 04 07'42''S; C. f. bimaculatus MAD500 Cfu500 MPEG 59 21'55.4''W Autazes, Uricurituba, Ilha - AM 03 34'47''S; C.f. bimaculatus MAD608 Cfu608 MPEG 59 07'50''W Santa Catarina - SC TERNA210, Cfu210, Cfu398, o † (27 14'32.42''S; C. f. fuscatus TERNA398,TERNA1068, Cfu1068, MNRJ 50 13'7.88''W) TERNA1349, Cachimbo470 Cfu1349, Cfu470 Rio Branco - AC UFAC1199, UFAC1297, Cfu1199, (09 57'32.3''S; C. f. beniensis MPEG UFAC273 Cfu1297, Cfu273 67 43'57.2''W) Monte Alegre - PA (2 3'14.72''S; C. f. fuscatior PEMA042, PEMA037 Cfu042, Cfu037 MPEG 54 10'24.49''W) Revista Brasileira de Ornitologia 26(4): 2018 Plumage polymorphism in Fuscous Flycatcher, Cnemotriccus fuscatus Vieira et al. v. 7.2.5, to confi rm the position of amplifi ed fragment. samples (Table 2), including all six subspecies. Th ese We then assessed if aminoacid sequence presented stop variable sites of the MC1R locus determined six non- codons and indels, which could indicate pseudogenes. Th e synonymous mutations for the codifi cation of amino potential association of variable sites with the plumage acids, A8G, S9R, S10N, S89N, V226I, and L240I morphotype of each species was confi rmed by visual (Table 3). None of these sites were associated with the inspection. We calculated Tajima's D (Tajima 1989) in coloration patterns of either the two groups or any of DnaSP (version 3.51, Rozas et al. 2003) to verify whether the subspecies. Tajima's D was not signifi cant (-1.603, the MC1R gene was under selection pressure in the two P > 0.05), indicating that the variation found in the groups. study locus in C. fuscatus is neutral, with a signal of recent demographic expansion, against the constant demographic model. All the sequences generated in RESULTS the present study were deposited in GenBank (www. ncbi.nlm.nih.gov) under access numbers MK102986 A total of 744 base pairs were sequenced for each of the through MK103006 (Table 3). 27 C. fuscatus samples, representing nucleotides 129– 873 of the MC1R gene of Gallus gallus, which includes all the sites known to be associated with plumage DISCUSSION polymorphisms in birds (Th eron et al. 2001). Only 21 samples were considered (pp >0.6) after the resolution Our study of Cnemotriccus fuscatus indicates that there is of the gametic phases (Harrigan et al. 2008, Table 2). In no clear association between the plumage polymorphism the BLAST (NCBI: National Center for Biotechnology found in this species and mutations of the MC1R gene. Information) analysis, the sequences were 95% similar to As in previous studies of bird species such as Phylloscopus that of Gallus gallus (Kerje et al. 2003) and 97% similar to toutinegras (MacDougall-Shackleton et al. 2003), that of Coereba fl aveola (Th eron et al. 2001). Lepidothrix coronata (Cheviron et al. 2006), Dendrocolaptes We identifi ed 22 variable sites in the 21 C. fuscatus platyrostris (Corso et al. 2013), Philomachus pugnax Table 2. MC1R variable sites found in the sequences of Cnemotriccus fuscatus. Nucleotidic sites 11 1 2 2 2 2 3 3 4 4 5666 6 7 7 Voucher – Subspecies Belly Plumage 1 2 2 2 7 3 7 7 1 4 67 12 6 9 0 3 4 78 1 2 5 3 5 9 5 8 2 2 3 3 66 87 5 8 4 3 8 67 8 3 Cfu008 - C. f. fumosus G C A G A C C C G C G C C T C C C/G T C G C C/A C Yellow Cfu117- C. f. fumosus . . . . . . . . . . . . . . . . . . . . . . . Yellow Cfu118 - C. f. fumosus . . . . . . . . . . . . . . . . . . . . . . . Yellow Cfu1410 - C. f. fumosus . . . . . . . . . . A T . . . . . . T . . . . Yellow Cfu359 - C. f. fumosus . . . . A/G . . . . . . . . . T . . . T G/A T . T Yellow Cfu225 - C. f. duidae . . . . . . . . . . . . . . T . . . T . . . T Yellow Cfu267- C. f. duidae . . . . . . . . . . A T . . . . . . T . . . C/T Yellow Cfu0976 - C. f. duidae . . . . G/A . . . . . G/A C/T . . . . . . T . . . . Yellow Cfu1021 - C. f. duidae . . . . A/G . . . . . . . . . . . . . C/T . . . . Yellow Cfu270 - C. f. duidae . . . . G . . . . . . . . . . . . . T . . . . Yellow Cfu210 - C. f. fuscatus . . . . . . . . . . . . . . . . . . . . . . . Yellow Cfu398 - C. f. fuscatus . . . . . . . . . . . . . . . . . . . . . . C/T Yellow Cfu1068 - C. f. fuscatus . . . . . . . . . . . . . . . . . . . . . . . Yellow Cfu273 - C. f. beniensis . G C G/A . . . . . . . . . . . C/A . . . . . . . White Cfu1297 - C. f. beniensis . . . . . . . C/T . . . . . . . . . . . . . . . White Cfu500 - C. f. bimaculatus A/G . . . . . . C/T . . . . . . . . . . . . . . . White Cfu608 - C. f. bimaculatus . . . . . . . . . . . . . . . . . . . . . . . White Cfu005 - C. f. bimaculatus . . . . G . . . A/G T/C . . C/T C C/T . . . . . . . . White Cfu042 - C. f. bimaculatus . . . . . . . . . . . . . . . . . . . . . . . White Cfu171 - C. f. bimaculatus . . . . . . . . . . . . . . . . . . . . . . . White Cfu042 - C. f. fuscatior . . . . . T/C T/C . . . . . . . . . . C/T . . . . C/T White Revista Brasileira de Ornitologia 26(4): 2018 Plumage polymorphism in Fuscous Flycatcher, Cnemotriccus fuscatus Vieira et al. Table 3. Position of non-synonymous variations within the amino acid Cnemotriccus fuscatus. GenBank access numbers for the samples analyzed. Amino acid positions Voucher – Subspecies Access number Belly Plumage GenBank Cfu008 - C. f. fumosus A S S S V L/I Yellow MK102986 Cfu117 - C. f. fumosus ...... Yellow MK102987 Cfu118 - C. f. fumosus ...... Yellow MK102988 Cfu1410 - C. f. fumosus ... N .. Yellow MK102989 Cfu359 - C. f. fumosus .... V/I . Yellow MK102990 Cfu225 - C. f. duidae ...... Yellow MK102991 Cfu267 - C. f. duidae ... N .. Yellow MK102992 Cfu0976 - C. f. duidae ... S/N .. Yellow MK102993 Cfu1021 - C. f. duidae ...... Yellow MK102994 Cfu270 - C. f. duidae ...... Yellow MK102995 Cfu210 - C. f. fuscatus ...... Yellow MK102996 Cfu398 - C. f. fuscatus ...... Yellow MK102997 Cfu1068 - C. f. fuscatus ...... Yellow MK102998 Cfu273 - C. f. beniensis G R S/N ... White MK102999 Cfu1297 - C. f. beniensis ...... White MK103000 Cfu500 - C. f. bimaculatus ...... White MK103001 Cfu608 - C. f. bimaculatus ...... White MK103002 Cfu005 - C. f. bimaculatus ...... White MK103003 Cfus042 - C. f. bimaculatus ...... White MK103004 Cfu171 - C. f. bimaculatus ...... White MK103005 Cfu042 - C. f. fuscatior ...... White MK103006 (Farrell et al. 2014) and the genus Antilophia (Luna et 2016), SRY-Box containing 10, SOX10 (Gunnarsson et al. al. 2018), our fi ndings reinforce the conclusion that 2011), Agouti protein, ASIP (Oribe et al. 2012, Zhang et this gene does not always play a role in the variation in al. 2013), and Corin (Bourgeois et al. 2016) genes, and plumage coloration found among populations or species. the proopiomelanocortin (POMC) gene cluster, which includes MC1R (Kang & Kim 2015). In this case, other genes or mechanisms may determine this variation, as observed in a number of birds (McLean In addition to genetics, the variation found in the & Stuart-Fox 2014). coloration of C. fuscatus may be related to environmental A number of new genes associated with plumage factors, given the diversity of habitats occupied by the coloration have been identifi ed in recent years, although species (Fig. 1). Uy et al. (2009), for example, found that natural selection may favor distinct coloration in diff erent they have been analyzed in only a few species (Oribe et al. 2012, Bourgeois et al. 2016). Miwa et al. (2007), habitats based on the existence of several population for example, found an association between mutations patterns, with habitats dominated by short-wavelength of the endothelin receptor B2 (EDNRB2) gene and the light (e.g., shaded woodland) favoring darker birds, and coloration of Cortunix japonica, with a non-synonymous habitats rich in long-wavelength light (e.g., forest clearings with direct sunlight) favor lighter-colored species. substitution that alters an amino acid (R332H) being associated with the “panda” pattern, in contrast with the Furthermore, the studied part of the gene MC1R standard “dotted white” pattern. Other genes that may be includes all the main sites that were showed in previous involved in pigmentation in birds include the tyrosinase- research with plumage polymorphism of birds (Mundy related protein 1, TYRP1 (Xu et al. 2013, Bourgeois et al. 2005, Cheviron et al. 2006). Overall, our results reinforce Revista Brasileira de Ornitologia 26(4): 2018 Plumage polymorphism in Fuscous Flycatcher, Cnemotriccus fuscatus Vieira et al. Galván I. & Jorge A. 2015. Th e rusty plumage coloration of juvenile the conclusion that understanding the evolution of Gyrfalcons is produced by pheomelanin and its expression is plumage coloration in C. fuscatus with varying patterns aff ected by an intracellular antioxidant. Journal of Raptor Research of eumelanin/pheomelanin pigmentation requires a more 49: 59‒65. profound investigation of the genes in the melanocortin García-Borrón J.C., Sánchez-Laorden B.L., Jiménez-Cervantes C. 2005. pathway and their potential variation, as well as other Melanocortin-1 receptor structure and functional regulation. Pigment Cell and Melanoma Research 18: 393‒410. loci and environmental factors. Unlike many other bird Gomez D. & Th éry M. 2004. Infl uence of ambient light on the species (see e.g., Cheviron et al. 2006, Corso et al. 2013, evolution of colour signals: comparative analysis of a Neotropical Farrell et al. 2014, Luna et al. 2018), the variation in the Rainforest bird community. Ecology Letters 7: 279‒284. plumage coloration of C. fuscatus does not appear to be Gunnarsson U., Kerje S., Bed'hom B., Sahlqvist A.-S., Ekwall O., Tixier-Boichard M., Kämpe O. & Andersson L. 2011. Th e dark related to mutations of the MC1R gene. brown plumage color in chickens is caused by an 8.3-kb deletion upstream of SOX10. Pigment Cell and Melanoma Research 24: 268‒274. ACKNOWLEDGEMENTS Harrigan R.J., Mazza M.E. & Sorenson M.D. 2008. Computation vs. cloning: evaluation of two methods for haplotype determination. Molecular Ecology Resources 8: 1239‒1248. We thank the Goeldi Museum (MPEG) and National Hewitt G.M. 1988. Hybrid zones: natural laboratories for evolutionary Museum (MNRJ) for providing samples. We are also studies. Trends in Ecology and Evolution 3: 158‒167. grateful to the Federal University of Pará (UFPA) for Hoekstra H. & Price T. 2004. Parallel evolution is in the genes. Science 303: 1779‒1781. infrastructure, the Institutional Program of Scientifi c Johnson J.A., Ambers A.D. & Burnham K.K. 2012. Genetics of Initiation Scholarships (PIBIC) for granting an plumage color in the Gyrfalcon (Falco rusticolus): analysis of the undergraduate scholarship, the CAPES Science Without melanocortin-1 receptor gene. Journal of Heredity 103: 315‒321 Borders (CSF) program for supporting overseas academic Kang D.Y. & Kim H.C. 2015. Functional relevance of three proopiomelanocortin (POMC) genes in darkening camoufl age, exchange and Stephen Ferrari for the revision of the blind-side hypermelanosis, and appetite of Paralichthys olivaceus. manuscript. A.A. is supported by a CNPq research Comparative Biochemistry and Physiology B: Biochemistry and productivity fellowship (# 306843/2016-1). Molecular Biology 179: 44‒56. Kerje S., Lind J., Schutz K., Jensen P. & Andersson L. 2003. Melanocortin 1-receptor (MC1R) mutations are associated with plumage colour in chicken. Animal Genetics 34: 241‒248. REFERENCES Legagneux P., Clark R.G., Guillemain M., Eraud C., Th éry M. & Bretagnolle V. 2012. 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Ornithology Research – Springer Journals
Published: Dec 1, 2018
Keywords: birds; MC1R gene; mutation; pigmentation; Tyrannidae
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