Recurrent Evolution of Melanism in South American Felids


Color polymorphism in closely related animal species provides an opportunity to study how the balance between natural selection and genetic drift shapes the evolution of appearance and form. The cat family, Felidae, is especially interesting; 13 of 37 extant species exhibit polymorphism for melanism, but evidence for any adaptive role is lacking, in part because the potential benefits of melanism to felid predators are not clear, and in part because the tools for genomic analysis of natural populations are limited. We identify the mutations responsible for melanism in three closely related South American wild felids, the pampas cat, the kodkod, and Geoffroy’s cat, then adapt a new approach for targeted genome sequencing to characterize molecular variation in the region surrounding each melanism mutation. We find that each mutation has developed independently, with strong evidence for natural selection in the black pampas cat, and reduced genetic variation in the entire population of kodkods. Our results demonstrate that some “black cats” are black not by chance, but by selection for a mutation that provides increased fitness.


Vyšlo v časopise: Recurrent Evolution of Melanism in South American Felids. PLoS Genet 11(2): e32767. doi:10.1371/journal.pgen.1004892
Kategorie: Research Article
prolekare.web.journal.doi_sk: 10.1371/journal.pgen.1004892

Souhrn

Color polymorphism in closely related animal species provides an opportunity to study how the balance between natural selection and genetic drift shapes the evolution of appearance and form. The cat family, Felidae, is especially interesting; 13 of 37 extant species exhibit polymorphism for melanism, but evidence for any adaptive role is lacking, in part because the potential benefits of melanism to felid predators are not clear, and in part because the tools for genomic analysis of natural populations are limited. We identify the mutations responsible for melanism in three closely related South American wild felids, the pampas cat, the kodkod, and Geoffroy’s cat, then adapt a new approach for targeted genome sequencing to characterize molecular variation in the region surrounding each melanism mutation. We find that each mutation has developed independently, with strong evidence for natural selection in the black pampas cat, and reduced genetic variation in the entire population of kodkods. Our results demonstrate that some “black cats” are black not by chance, but by selection for a mutation that provides increased fitness.


Zdroje

1. Caro TIM (2005) The Adaptive Significance of Coloration in Mammals. BioScience 55: 125–136.

2. Hoekstra HE (2006) Genetics, development and evolution of adaptive pigmentation in vertebrates. Heredity (Edinb) 97: 222–234. 16823403

3. Hubbard JK, Uy JA, Hauber ME, Hoekstra HE, Safran RJ (2010) Vertebrate pigmentation: from underlying genes to adaptive function. Trends Genet 26: 231–239. doi: 10.1016/j.tig.2010.02.002 20381892

4. Johnson WE, Eizirik E, Pecon-Slattery J, Murphy WJ, Antunes A et al. (2006) The late Miocene radiation of modern Felidae: a genetic assessment. Science 311: 73–77. 16400146

5. Werdelin L, Yamaguchi N, Johnson WE, O’Brien SJ (2010) Phylogeny and evolution of cats (Felidae). In: Macdonald DW, Loveridge AJ, editors. Biology and conservation of wild felids. Oxford; New York: Oxford University Press. pp. 59–82.

6. Robinson R (1990) Homologous genetic variation in the Felidae. Genetica 46: 1–31.

7. Sunquist ME, Sunquist F (2002) Wild Cats of the World. Chicago, IL: The University of Chicago Press. 25057650

8. Schneider A, David VA, Johnson WE, O’Brien SJ, Barsh GS et al. (2012) How the Leopard Hides Its Spots: ASIP Mutations and Melanism in Wild Cats. PLoS One 7: e50386. doi: 10.1371/journal.pone.0050386 23251368

9. Allen WL, Cuthill IC, Scott-Samuel NE, Baddeley R (2011) Why the leopard got its spots: relating pattern development to ecology in felids. Proc Biol Sci 278: 1373–1380. doi: 10.1098/rspb.2010.1734 20961899

10. Majerus ME, Mundy NI (2003) Mammalian melanism: natural selection in black and white. Trends Genet 19: 585–588. 14585605

11. Majerus MEN, Brakefield PM (1998) Melanism: evolution in action. Oxford, NY: Oxford University Press. 25506963

12. Anderson TM, vonHoldt BM, Candille SI, Musiani M, Greco C et al. (2009) Molecular and evolutionary history of melanism in North American gray wolves. Science 323: 1339–1343. doi: 10.1126/science.1165448 19197024

13. Kawanishi K, Sunquist ME, Eizirik E, Lynam AJ, Ngoprasert D et al. (2010) Near fixation of melanism in leopards of the Malay Peninsula. Journal of Zoology 282: 201–206.

14. Dunstone N, Durbin L, Wyllie I, Freer R, Jamett GA et al. (2002) Spatial organization, ranging behaviour and habitat use of the kodkod (Oncifelis guigna) in southern Chile. Journal of Zoology 257: 1–11.

15. Napolitano CG (2012) Filogeografía, inferencia demográfica y genética de la conservación del felino Leopardus guigna en el sur de sudamérica. Programa de doctorado en Ciencias Silvoagropecuarias y Veterinarias, Universidad de Chile 255 pp.

16. Napolitano C, Johnson W, Sanderson J, O,ÄôBrien S, Rus H, A et al. (2014) Phylogeography and population history of Leopardus guigna, the smallest American felid. Conserv Genet 15: 631–653.

17. Sanderson J, Sunquist M.E., Iriarte A.W. (2002) Natural history and landscape-use of guignas (Oncifelis guigna) on Isla Grande de Chiloe, Chile. Journal of Mammalogy 608–613.

18. Trigo TC, Freitas TR, Kunzler G, Cardoso L, Silva JC et al. (2008) Inter-species hybridization among Neotropical cats of the genus Leopardus, and evidence for an introgressive hybrid zone between L. geoffroyi and L. tigrinus in southern Brazil. Mol Ecol 17: 4317–4333. doi: 10.1111/j.1365-294X.2008.03919.x 18785898

19. Trigo TC, Schneider A, de Oliveira TG, Lehugeur LM, Silveira L et al. (2013) Molecular data reveal complex hybridization and a cryptic species of neotropical wild cat. Curr Biol 23: 2528–2533. doi: 10.1016/j.cub.2013.10.046 24291091

20. George RD, McVicker G, Diederich R, Ng SB, MacKenzie AP et al. (2011) Trans genomic capture and sequencing of primate exomes reveals new targets of positive selection. Genome Research 21: 1686–1694. doi: 10.1101/gr.121327.111 21795384

21. Day K, Song J, Absher D (2014) Targeted sequencing of large genomic regions with CATCH-Seq. PloS One Unpublished: (in review).

22. Klungland H, Vage DI (2003) Pigmentary switches in domestic animal species. Ann N Y Acad Sci 994: 331–338. 12851333

23. Kaelin CB, Barsh GS (2012) Molecular Genetics of Coat Colour, Texture and Length in the Dog. In: Ostrander EA, Ruvinsky A, editors. The Genetics of the Dog, 2nd ed. Boston, MA: CABI. pp. 57–80.

24. Simon JD, Peles D, Wakamatsu K, Ito S (2009) Current challenges in understanding melanogenesis: bridging chemistry, biological control, morphology, and function. Pigment Cell Melanoma Res 22: 563–579. doi: 10.1111/j.1755-148X.2009.00610.x 19627559

25. Jackson IJ (1994) Molecular and developmental genetics of mouse coat color. Annu Rev Genet 28: 189–217. 7893123

26. Suzuki H (2013) Evolutionary and phylogeographic views on Mc1r and Asip variation in mammals. Genes Genet Syst 88: 155–164. 24025244

27. Candille SI, Kaelin CB, Cattanach BM, Yu B, Thompson DA et al. (2007) A beta-defensin mutation causes black coat color in domestic dogs. Science 318: 1418–1423. 17947548

28. Gunn TM, Miller KA, He L, Hyman RW, Davis RW et al. (1999) The mouse mahogany locus encodes a transmembrane form of human attractin. Nature 398: 152–156. 10086356

29. He L, Lu XY, Jolly AF, Eldridge AG, Watson SJ et al. (2003) Spongiform degeneration in mahoganoid mutant mice. Science 299: 710–712. 12560552

30. McNulty JC, Jackson PJ, Thompson DA, Chai B, Gantz I et al. (2005) Structures of the agouti signaling protein. J Mol Biol 346: 1059–1070. 15701517

31. Robbins LS, Nadeau JH, Johnson KR, Kelly MA, Roselli-Rehfuss L et al. (1993) Pigmentation phenotypes of variant extension locus alleles result from point mutations that alter MSH receptor function. Cell 72: 827–834. 8458079

32. Vage DI, Lu D, Klungland H, Lien S, Adalsteinsson S et al. (1997) A non-epistatic interaction of agouti and extension in the fox, Vulpes vulpes. Nat Genet 15: 311–315. 9054949

33. Gray SM, McKinnon JS (2007) Linking color polymorphism maintenance and speciation. Trends Ecol Evol 22: 71–79. 17055107

34. Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29: 1969–1973. doi: 10.1093/molbev/mss075 22367748

35. Eizirik E, Yuhki N, Johnson WE, Menotti-Raymond M, Hannah SS et al. (2003) Molecular genetics and evolution of melanism in the cat family. Curr Biol 13: 448–453. 12620197

36. He L, Eldridge AG, Jackson PK, Gunn TM, Barsh GS (2003) Accessory proteins for melanocortin signaling: attractin and mahogunin. Ann N Y Acad Sci 994: 288–298. 12851328

37. Leffler EM, Bullaughey K, Matute DR, Meyer WK, Segurel L et al. (2012) Revisiting an old riddle: what determines genetic diversity levels within species? PLoS Biol 10: e1001388. doi: 10.1371/journal.pbio.1001388 22984349

38. Echeverria C, Coomes D, Salas J, Rey-Benayas JM, Lara A et al. (2006) Rapid deforestation and fragmentation of Chilean Temperate Forests. Biological Conservation 130: 481–494.

39. Pontius JU, O’Brien SJ (2007) Genome Annotation Resource Fields—GARFIELD: a genome browser for Felis catus. J Hered 98: 386–389. 17646276

40. Mullikin JC, Hansen NF, Shen L, Ebling H, Donahue WF et al. (2010) Light whole genome sequence for SNP discovery across domestic cat breeds. BMC Genomics 11: 406. doi: 10.1186/1471-2164-11-406 20576142

41. Zhi D, Raphael BJ, Price AL, Tang H, Pevzner PA (2006) Identifying repeat domains in large genomes. Genome Biol 7: R7. 16507140

42. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754–1760. doi: 10.1093/bioinformatics/btp324 19451168

43. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078–2079. doi: 10.1093/bioinformatics/btp352 19505943

44. Genome Sequencing and Analysis Group (2012) Best Practice Variant Detection with the GATK v3. Cambridge, MA: Broad Institute. doi: 10.1111/cob.12003 23271062

45. Browning SR, Browning BL (2007) Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. Am J Hum Genet 81: 1084–1097. 17924348

46. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451–1452. doi: 10.1093/bioinformatics/btp187 19346325

47. Sabeti PC, Reich DE, Higgins JM, Levine HZ, Richter DJ et al. (2002) Detecting recent positive selection in the human genome from haplotype structure. Nature 419: 832–837. 12397357

48. Gautier M, Vitalis R (2012) rehh: an R package to detect footprints of selection in genome-wide SNP data from haplotype structure. Bioinformatics 28: 1176–1177. doi: 10.1093/bioinformatics/bts115 22402612

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