#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Fixation of genetic variation and optimization of gene expression: The speed of evolution in isolated lizard populations undergoing Reverse Island Syndrome


Autoři: Maria Buglione aff001;  Simona Petrelli aff001;  Valeria Maselli aff001;  Martina Trapanese aff001;  Marco Salvemini aff001;  Serena Aceto aff001;  Anna Di Cosmo aff001;  Domenico Fulgione aff001
Působiště autorů: Department of Biology, University of Naples Federico II Naples, Naples, Italy aff001
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0224607

Souhrn

The ecological theory of island biogeography suggests that mainland populations should be more genetically divergent from those on large and distant islands rather than from those on small and close islets. Some island populations do not evolve in a linear way, but the process of divergence occurs more rapidly because they undergo a series of phenotypic changes, jointly known as the Island Syndrome. A special case is Reversed Island Syndrome (RIS), in which populations show drastic phenotypic changes both in body shape, skin colouration, age of sexual maturity, aggressiveness, and food intake rates. The populations showing the RIS were observed on islets nearby mainland and recently raised, and for this they are useful models to study the occurrence of rapid evolutionary change. We investigated the timing and mode of evolution of lizard populations adapted through selection on small islets. For our analyses, we used an ad hoc model system of three populations: wild-type lizards from the mainland and insular lizards from a big island (Capri, Italy), both Podarcis siculus siculus not affected by the syndrome, and a lizard population from islet (Scopolo) undergoing the RIS (called P. s. coerulea because of their melanism). The split time of the big (Capri) and small (Scopolo) islands was determined using geological events, like sea-level rises. To infer molecular evolution, we compared five complete mitochondrial genomes for each population to reconstruct the phylogeography and estimate the divergence time between island and mainland lizards. We found a lower mitochondrial mutation rate in Scopolo lizards despite the phenotypic changes achieved in approximately 8,000 years. Furthermore, transcriptome analyses showed significant differential gene expression between islet and mainland lizard populations, suggesting the key role of plasticity in these unpredictable environments.

Klíčová slova:

Gene expression – Haplotypes – Phylogenetic analysis – Population genetics – Evolutionary genetics – Islands – Mitochondrial DNA – Lizards


Zdroje

1. Emerson BC (2002) Evolution on oceanic islands: molecular phylogenetic approaches to understanding pattern and process. Mol Ecol 11: 951–966. doi: 10.1046/j.1365-294x.2002.01507.x 12030975

2. Lachaise D, Harry M, Solignac M, Lemeunier F, Benassi V, Cariou ML (2000) Evolutionary novelties in islands: Drosophila santomea, a new melanogaster sister species from Sao Tome. Proc Biol Sci 267: 1487–1495. doi: 10.1098/rspb.2000.1169 11007323

3. Hofman CA, Rick TC, Hawkins MTR, Funk WC, Ralls K, Boser CL, et al. (2015) Mitochondrial Genomes Suggest Rapid Evolution of Dwarf California Channel Islands Foxes (Urocyon littoralis). PLoS One 10.

4. Jaenike JR (1973) A steady state model of genetic polymorphism on islands. The American Naturalist 107: 793–795.

5. Johnson KP (2003) Island biogeography and evolution: Genetic divergence and speciation of island taxa. Comments Theor Biol 8: 339–356.

6. Perez-Cembranos A, Leon A, Perez-Mellado V (2016) Omnivory of an Insular Lizard: Sources of Variation in the Diet of Podarcis lilfordi (Squamata, Lacertidae). PLoS One 11: e0148947. doi: 10.1371/journal.pone.0148947 26871439

7. Perez-Mellado V, Barbadillo LJ, Barahona F, Brown RP, Corti C, Guerriero F, et al. (1993) A systematic survey of the Iberian rock lizard, Lacerta (Archaeolacerta) monticola. In: Valakos D, hme W, Perez-Mellado V, Maragou P, editors. Lacertids of the Mediterranean region: a biological approach. Athens: Hellenic Zoological Society. pp. 85–105.

8. Sagonas K, Pafilis P, Lymberakis P, Donihue CM, Herrel A, Valakos ED (2014) Insularity affects head morphology, bite force and diet in a Mediterranean lizard. Biological Journal of the Linnean Society 112: 469–484.

9. Sagonas K, Pafilis P, Lymberakis P, Valakos ED (2015) Trends and patterns in the feeding ecology of the widespread Balkan lizard Lacerta trilineata (Squamata: Lacertidae) in insular and continental Greece. North-West J Zool 11: 117–126.

10. Sagonas K, Pafilis P, Valakos ED (2015) Effects of insularity on digestion: living on islands induces shifts in physiological and morphological traits in island reptiles. Naturwissenschaften 102: 55. doi: 10.1007/s00114-015-1301-8 26319572

11. Blondel J, Aronson J (1999) Biology and wildlife of the Mediterranean region.; Press OU, editor. New York.

12. Clegg SM, Owens PF (2002) The ‘island rule’ in birds: medium body size and its ecological explanation. Proceedings of the Royal Society of London Series B: Biological Sciences 269: 1359–1365. doi: 10.1098/rspb.2002.2024 12079659

13. Grant PR (1998) Patterns on islands and microevolution. In: Grant PR, editor. Evolution on islands. Oxford, UK: Oxford University Press. pp. 1–17.

14. Losos JB, Ricklefs RE (2009) Adaptation and diversification on islands. Nature 457: 830–836. doi: 10.1038/nature07893 19212401

15. McNab BK (1994) Resource use and the survival of land and freshwater vertebrates on oceanic islands. Am Nat 144: 643–660.

16. Whittaker RJ, Fernandez-Palacios JM (2007) Island biogeography. Ecology, evolution, and conservation. Oxford: Oxford University Press.

17. Raia P, Meiri S (2011) The tempo and mode of evolution: body sizes of island mammals. Evolution 65: 1927–1934. doi: 10.1111/j.1558-5646.2011.01263.x 21729048

18. Thomas GH, Meiri S, Phillimore AB (2009) Body size diversification in Anolis: Novel environments and island effects. Evolution 63: 2017–2030. doi: 10.1111/j.1558-5646.2009.00694.x 19453734

19. Millien V (2006) Morphological evolution is accelerated among island mammals. PLoS Biology 4: e321. doi: 10.1371/journal.pbio.0040321 16968136

20. Millien V (2011) Mammals evolve faster on smaller islands. Evolution 65: 1935–1944. doi: 10.1111/j.1558-5646.2011.01268.x 21729049

21. Aubret F (2015) Island colonisation and the evolutionary rates of body size in insular neonate snakes. Heredity (Edinb) 115: 349–356.

22. Fulgione D, Lega C, Trapanese M, Buglione M (2015) Genetic factors implied in melanin-based coloration of the Italian wall lizard. Journal of Zoology 296: 278–285.

23. Monti DM, Raia P, Vroonen J, Maselli V, Van Damme R, Fulgione D (2013) Physiological change in an insular lizard population confirms the reversed island syndrome. Biological Journal of the Linnean Society 108: 144–150.

24. Raia P, Guarino FM, Turano M, Polese G, Rippa D, Carotenuto F, et al. (2010) The blue lizard spandrel and the island syndrome. BMC Evol Biol 10: 289. doi: 10.1186/1471-2148-10-289 20854657

25. Trapanese M, Buglione M, Maselli V, Petrelli S, Aceto S, Fulgione D (2017) The first transcriptome of Italian wall lizard, a new tool to infer about the Island Syndrome. PLoS One 12: e0185227. doi: 10.1371/journal.pone.0185227 28953924

26. Bagnara JT, Fernandez PJ, Fujii R (2007) On the blue coloration of vertebrates. Pigment Cell Res 20: 14–26. doi: 10.1111/j.1600-0749.2006.00360.x 17250544

27. Corti C, Capula M, Luiselli L, Sindaco R, Razzetti E (2011) Fauna d’Italia. Reptilia. Bologna: Calderini XII.

28. Wolstenholme DR (1992) Animal mitochondrial DNA: structure and evolution. Int Rev Cytol 141: 173–216. doi: 10.1016/s0074-7696(08)62066-5 1452431

29. Eo SH, DeWoody JA (2010) Evolutionary rates of mitochondrial genomes correspond to diversification rates and to contemporary species richness in birds and reptiles. Proc Biol Sci 277: 3587–3592. doi: 10.1098/rspb.2010.0965 20610427

30. Bernardo PH, Sanchez-Ramirez S, Sanchez-Pacheco SJ, Alvarez-Castaneda ST, Aguilera-Miller EF, Mendez-de la Cruz FR, et al. (2019) Extreme mito-nuclear discordance in a peninsular lizard: the role of drift, selection, and climate. Heredity (Edinb).

31. Morales HE, Pavlova A, Joseph L, Sunnucks P (2015) Positive and purifying selection in mitochondrial genomes of a bird with mitonuclear discordance. Mol Ecol 24: 2820–2837. doi: 10.1111/mec.13203 25876460

32. Schena M, Shalon D, Davis RW, Brown PO (1995) Quantitative monitoring of gene expression patterns with a complementary DNA microarray. Science 270: 467–470. doi: 10.1126/science.270.5235.467 7569999

33. Andreone F, Guarino F (2003) Giant and long-lived: age structure in Macroscincus coctei, an extinct skink from Cape Verde. Amphibia-Reptilia 24: 459–470.

34. Guarino F, Lunardi S, Carlomagno M, Mazzotti S (2003) A skeletochronological study of growth, longevity, and age at sexual maturity in a population of Rana latastei (Amphibia, Anura). J Biosci 28: 775–782. doi: 10.1007/bf02708438 14660877

35. Fulgione D, Buglione M, Rippa D, Trapanese M, Petrelli S, Monti DM, et al. (2019) Selection for background matching drives sympatric speciation in Wall Gecko. Scientific Reports 9: 1288. doi: 10.1038/s41598-018-37587-3 30718570

36. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30: 2114–2120. doi: 10.1093/bioinformatics/btu170 24695404

37. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, et al. (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647–1649. doi: 10.1093/bioinformatics/bts199 22543367

38. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574. doi: 10.1093/bioinformatics/btg180 12912839

39. Guindon S, Gascuel O (2003) A Simple, Fast, and Accurate Algorithm to Estimate Large Phylogenies by Maximum Likelihood. Systematic Biology 52: 696–704. doi: 10.1080/10635150390235520 14530136

40. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14: 817–818. doi: 10.1093/bioinformatics/14.9.817 9918953

41. Rambaut A, Suchard M, Xie D, Drummond A (2014) Tracer v1.4. http://beast.bio.ed.ac.uk/Tracer.

42. Bouckaert RR (2010) DensiTree: making sense of sets of phylogenetic trees. Bioinformatics 26: 1372–1373. doi: 10.1093/bioinformatics/btq110 20228129

43. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7: 214. doi: 10.1186/1471-2148-7-214 17996036

44. Lambeck K, Antonioli F, Purcell A, Silenzi S (2004) Sea-level change along the Italian coast for the past 10,000 yr. Quaternary Science Reviews 23: 1567–1598.

45. Lambeck K, Antonioli F, Anzidei M, Ferranti L, Leoni G, Scicchitano G, et al. (2011) Sea level change along the Italian coast during the Holocene and projections for the future. Quaternary International 232: 250–257.

46. McDonald JH, Kreitman M (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351: 652–654. doi: 10.1038/351652a0 1904993

47. Nei M (1987) Molecular Evolutionary Genetics. New York: Columbia University Press.

48. 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

49. Rand DM, Kann LM (1996) Excess amino acid polymorphism in mitochondrial DNA: contrasts among genes from Drosophila, mice, and humans. Mol Biol Evol 13: 735–748. doi: 10.1093/oxfordjournals.molbev.a025634 8754210

50. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, et al. (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29: 644–652. doi: 10.1038/nbt.1883 21572440

51. Waterhouse RM, Seppey M, Simao FA, Manni M, Ioannidis P, Klioutchnikov G, et al. (2017) BUSCO applications from quality assessments to gene prediction and phylogenomics. Mol Biol Evol.

52. Andrade P, Pinho C, Perez IdLG, Afonso S, Brejcha J, Rubin CJ, et al. (2019) Regulatory changes in pterin and carotenoid genes underlie balanced color polymorphisms in the wall lizard. Proc Natl Acad Sci U S A 116: 5633–5642. doi: 10.1073/pnas.1820320116 30819892

53. Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12: 323. doi: 10.1186/1471-2105-12-323 21816040

54. Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25. doi: 10.1186/gb-2009-10-3-r25 19261174

55. Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139–140. doi: 10.1093/bioinformatics/btp616 19910308

56. Musacchia F, Basu S, Petrosino G, Salvemini M, Sanges R (2015) Annocript: a flexible pipeline for the annotation of transcriptomes able to identify putative long noncoding RNAs. Bioinformatics 31: 2199–2201. doi: 10.1093/bioinformatics/btv106 25701574

57. Petrella V, Aceto S, Musacchia F, Colonna V, Robinson M, Benes V, et al. (2015) De novo assembly and sex-specific transcriptome profiling in the sand fly Phlebotomus perniciosus (Diptera, Phlebotominae), a major Old World vector of Leishmania infantum. BMC Genomics 16: 847. doi: 10.1186/s12864-015-2088-x 26493315

58. Fay JC, Wyckoff GJ, Wu CI (2001) Positive and negative selection on the human genome. Genetics 158: 1227–1234. 11454770

59. Raia P, Carotenuto F, Passaro F, Fulgione D, Fortelius M (2012) Ecological specialization in fossil mammals explains Cope's rule. American Naturalist 179: 328–337. doi: 10.1086/664081 22322221

60. Eldredge N, Thompson JN, Brakefield PM, Gavrilets S, Jablonski D, Jackson JBC, et al. (2005) The dynamics of evolutionary stasis. Paleobiology 31: 133–145.

61. Eldredge N, Gould SJ (1972) Punctuated equilibria: An alternative to phyletic gradualism. In: Schopf TJM, editor. Models in Paleobiology. San Francisco: Freeman. pp. 82–115.

62. Paenke I, Sendhoff B, Kawecki TJ (2007) Influence of plasticity and learning on evolution under directional selection. Am Nat 170: E47–58. doi: 10.1086/518952 17874367

63. Duncan EJ, Gluckman PD, Dearden PK (2014) Epigenetics, plasticity, and evolution: How do we link epigenetic change to phenotype? J Exp Zool B Mol Dev Evol 322: 208–220. doi: 10.1002/jez.b.22571 24719220

64. Ghalambor CK, Hoke KL, Ruell EW, Fischer EK, Reznick DN, Hughes KA (2015) Non-adaptive plasticity potentiates rapid adaptive evolution of gene expression in nature. Nature 525: 372–375. doi: 10.1038/nature15256 26331546

65. Fulgione D, Guglielmi S, Odierna G, Rippa D, Caliendo M, Rastogi R (2008) Morphological Differentiation and Genetic Structure in Island Lizard Populations. Zoological Science 25: 465–474. doi: 10.2108/zsj.25.465 18558798

66. Jin Y, Wo Y, Tong H, Song S, Zhang L, Brown RP (2018) Evolutionary analysis of mitochondrially encoded proteins of toad-headed lizards, Phrynocephalus, along an altitudinal gradient. BMC Genomics 19: 185. doi: 10.1186/s12864-018-4569-1 29510674

67. Pavlova A, Gan HM, Lee YP, Austin CM, Gilligan DM, Lintermans M, et al. (2017) Purifying selection and genetic drift shaped Pleistocene evolution of the mitochondrial genome in an endangered Australian freshwater fish. Heredity (Edinb) 118: 466–476.

68. Yu L, Wang X, Ting N, Zhang Y (2011) Mitogenomic analysis of Chinese snub-nosed monkeys: Evidence of positive selection in NADH dehydrogenase genes in high-altitude adaptation. Mitochondrion 11: 497–503. doi: 10.1016/j.mito.2011.01.004 21292038

69. Ancel LW (2000) Undermining the Baldwin expediting effect: does phenotypic plasticity accelerate evolution? Theor Popul Biol 58: 307–319. doi: 10.1006/tpbi.2000.1484 11162789

70. Ghalambor CK, McKay JK, Carroll SP, Reznick DN (2007) Adaptive versus non‐adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Functional Ecology 21: 394–407.

71. Price TD, Qvarnstrom A, Irwin DE (2003) The role of phenotypic plasticity in driving genetic evolution. Proc Biol Sci 270: 1433–1440. doi: 10.1098/rspb.2003.2372 12965006

72. Wright S (1931) Evolution in Mendelian Populations. Genetics 16: 97–159. 17246615

73. Roff DA (1994) The evolution of flightlessness: Is history important? Evolutionary Ecology 8: 639–657.

74. Omland KE (1997) Examining Two Standard Assumptions of Ancestral Reconstructions: Repeated Loss of Dichromatism in Dabbling Ducks (Anatini). Evolution 51: 1636–1646. doi: 10.1111/j.1558-5646.1997.tb01486.x 28568615

75. Grant PR (1999) Ecology and evolution of Darwin’s finches. Princeton: Princeton University Press.

76. Adler GH, Levins R (1994) The island syndrome in rodent populations. Q Rev Biol 69: 473–490. doi: 10.1086/418744 7855232

77. Bossdorf O, Richards CL, Pigliucci M (2008) Epigenetics for ecologists. Ecol Lett 11: 106–115. doi: 10.1111/j.1461-0248.2007.01130.x 18021243

78. Richards EJ (2008) Population epigenetics. Curr Opin Genet Dev 18: 221–226. doi: 10.1016/j.gde.2008.01.014 18337082

79. Scoville AG, Barnett LL, Bodbyl-Roels S, Kelly JK, Hileman LC (2011) Differential regulation of a MYB transcription factor is correlated with transgenerational epigenetic inheritance of trichome density in Mimulus guttatus. New Phytol 191: 251–263. doi: 10.1111/j.1469-8137.2011.03656.x 21352232

80. Zhang YY, Fischer M, Colot V, Bossdorf O (2013) Epigenetic variation creates potential for evolution of plant phenotypic plasticity. New Phytol 197: 314–322. doi: 10.1111/nph.12010 23121242

81. Champagne FA (2013) Epigenetics and developmental plasticity across species. Dev Psychobiol 55: 33–41. doi: 10.1002/dev.21036 22711291

82. Hu J, Barrett RDH (2017) Epigenetics in natural animal populations. J Evol Biol 30: 1612–1632. doi: 10.1111/jeb.13130 28597938

83. Thorson JLM, Smithson M, Beck D, Sadler-Riggleman I, Nilsson E, Dybdahl M, et al. (2017) Epigenetics and adaptive phenotypic variation between habitats in an asexual snail. Sci Rep 7.


Článok vyšiel v časopise

PLOS One


2019 Číslo 11
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#