The population genetics of crypsis in vertebrates: recent insights from mice, hares, and lizards.
Journal
Heredity
ISSN: 1365-2540
Titre abrégé: Heredity (Edinb)
Pays: England
ID NLM: 0373007
Informations de publication
Date de publication:
01 2020
01 2020
Historique:
received:
12
04
2019
accepted:
25
07
2019
revised:
16
07
2019
pubmed:
11
8
2019
medline:
20
5
2021
entrez:
11
8
2019
Statut:
ppublish
Résumé
By combining well-established population genetic theory with high-throughput sequencing data from natural populations, major strides have recently been made in understanding how, why, and when vertebrate populations evolve crypsis. Here, we focus on background matching, a particular facet of crypsis that involves the ability of an organism to conceal itself through matching its color to the surrounding environment. While interesting in and of itself, the study of this phenotype has also provided fruitful population genetic insights into the interplay of strong positive selection with other evolutionary processes. Specifically, and predicated upon the findings of previous candidate gene association studies, a primary focus of this recent literature involves the realization that the inference of selection from DNA sequence data first requires a robust model of population demography in order to identify genomic regions which do not conform to neutral expectations. Moreover, these demographic estimates provide crucial information about the origin and timing of the onset of selective pressures associated with, for example, the colonization of a novel environment. Furthermore, such inference has revealed crypsis to be a particularly useful phenotype for investigating the interplay of migration and selection-with examples of gene flow constraining rates of adaptation, or alternatively providing the genetic variants that may ultimately sweep through the population. Here, we evaluate the underlying evidence, review the strengths and weaknesses of the many population genetic methodologies used in these studies, and discuss how these insights have aided our general understanding of the evolutionary process.
Identifiants
pubmed: 31399719
doi: 10.1038/s41437-019-0257-4
pii: 10.1038/s41437-019-0257-4
pmc: PMC6906368
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
1-14Références
Alexander DH, Novembre J, Lange K (2009) Fast model-based estimation of ancestry in unrelated individuals. Genome Res 19:1655–1664
pmcid: 2752134
pubmed: 19648217
Barbosa-Morais NL, Irimia M, Pan Q, Xiong HY, Gueroussov S, Lee LJ et al. (2012) The evolutionary landscape of alternative splicing in vertebrate species. Science 338:1587–1593
pubmed: 23258890
Barrett RDH, Hoekstra HE (2011) Molecular spandrels: tests of adaptation at the genetic level. Nat Rev Genet 12:767–780
pubmed: 22005986
Barrett RDH, Laurent S, Mallarino R, Pfeifer SP, Xu CCY, Foll MF et al. (2019) Linking a mutation to survival in wild mice. Science 363:499–504
pubmed: 30705186
Barron DG, Brawn JD, Weatherhead PJ (2010) Meta-analysis of transmitter effects on avian behaviour and ecology. Methods Ecol Evol 1:180–187
Barton NH (1998) The effect of hitch-hiking on neutral genealogies. Genet Res 72:123–133
Bedford NL, Hoekstra HE (2015) Peromyscus mice as a model for studying natural variation. eLife 4:e06813
pmcid: 4470249
Benson SB (1933) Concealing coloration among some desert rodents of the Southwestern United States. Univ Calif Publ Zool 40:1–70
Bi K, Linderoth T, Vanderpool D, Good JM, Nielsen R, Moritz C (2013) Unlocking the vault: next-generation museum population genomics. Mol Ecol 22:5966–5968
Bi K, Linderoth T, Singhal S, Vanderpool D, Patton JL, Nielsen R, Moritz C, Good JM (2019) Temporal genomic contrasts reveal rapid evolutionary responses in an alpine mammal during recent climate change. PLoS Genet 15:e1008119
pmcid: 6519841
pubmed: 6519841
Caro T (2005) The adaptive significance of coloration in mammals. Bioscience 55:125
Caro T, Stoddard MC, Stuart-Fox D (2017) Animal coloration research: why it matters. Philos Trans R Soc B 372:20160333
Cheng E, Hodges KE, Melo-Ferreira J, Alves PC, Mills LS (2014) Conservation implications of the evolutionary history and genetic diversity hotspots of the snowshoe hare. Mol Ecol 23:2929–2942
pubmed: 24814937
Comeron JM (2017) Background selection as a null hypothesis in population genomics: insights and challenges from Drosophila studies. Philos Trans R Soc B 372(1736):pii: 20160471
Cook LM, Saccheri IJ (2013) The peppered moth and industrial melanism: evolution of a natural selection case study. Heredity 110:207–212
pubmed: 23211788
Corl A, Bi K, Luke C, Challa AS, Stern AJ, Sinervo B, Nielsen R (2018) The genetic basis of adaptation following plastic changes in coloration in a novel environment. Curr Biol 28:2970–2977
pubmed: 30197088
Cott HB (1940) Adaptive coloration in animals. Oxford University Press, Oxford
Crisci JL, Poh YP, Mahajan S, Jensen JD (2013) The impact of equilibrium assumptions on tests of selection. Front Genet 4:235
pmcid: 3822286
pubmed: 24273554
DeGiorgio M, Huber CD, Hubisz MJ, Hellmann I, Nielsen R (2016) SweepFinder2: increased sensitivity, robustness, and flexibility. Bioinformatics 32:1895–1897
pubmed: 27153702
DePristo M, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C et al. (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 43:491–498
pmcid: 3083463
pubmed: 3083463
Des Roches S, Sollmann R, Calhoun K, Rothstein AP, Rosenblum EB (2017) Survival by genotype: patterns at Mc1r are not black and white at the White Sands ecotone. Mol Ecol 26:320–329
Dice LR, Blossom PM (1937) Studies of mammalian ecology in south-western North America with special reference to the colors of desert animals. Carne Inst Wash Publ 485:1–129
Domingues VS, Poh YP, Peterson BK, Pennings PS, Jensen JD, Hoekstra HE (2012) Evidence of adaptation from ancestral variation in young populations of beach mice. Evolution 66:3209–3223
Endler JA (1981) An overview of the relationships between mimicry and crypsis. Biol J Linn Soc 16:25–21
Endler JA, Mappes J (2017) The current and future state of animal coloration research. Philos Trans R Soc B 372:20160352
Excoffier L, Dupanloup I, Huerta-Sanchez E, Sousa VC, Foll M (2013) Robust demographic inference from genomic and SNP data. PLoS Genet 9:e1003905
pmcid: 3812088
pubmed: 3812088
Fariello MI, Boitard S, Naya H, San Cristobal M, Servin B (2013) Detecting signatures of selection through haplotype differentiation among hierarchically structured populations. Genetics 193:929–941
pmcid: 3584007
pubmed: 3584007
Fisher RA (1930) The genetical theory of natural selection: a complete variorum edition. Oxford University Press, Oxford
Gutenkunst RN, Hernandez RD, Williamson SH, Bustamante CD (2009) Inferring the joint demographic history of multiple populations from multidimensional SNP frequency data. PLoS Genet 5:e1000695
pmcid: 2760211
pubmed: 2760211
Habel JC, Husemann M, Finger A, Danley PD, Zachos FE (2014) The relevance of time series in molecular ecology and conservation biology. Biol Rev Camb Philos Soc 89:484–492
pubmed: 24251767
Haldane JBS (1927) A mathematical theory of natural and artificial selection. Math Proc Camb Philos Soc 23:607
Haldane JBS (1930) A mathematical theory of natural and artificial selection. VI. Isolation. Proc Camb Philos Soc 26:220–230
Hardwick KM, Harmon LJ, Hardwick SD, Rosenblum EB (2015) When field experiments yield unexpected results: lessons learned from measuring selection in White Sands lizards. PLoS ONE 10:e0118560
pmcid: 4340912
pubmed: 25714838
Harris RB, Sackman AM, Jensen JD (2018) On the unfounded enthusiasm for soft selective sweeps II: examining recent evidence from humans, flies, and viruses. PLoS Genet 14:e1007859
pmcid: 6336318
pubmed: 30592709
Hermisson J, Pennings PS (2005) Soft sweeps: molecular population genetics of adaptation from standing genetic variation. Genetics 169:2335–2352
pmcid: 1449620
pubmed: 15716498
Hodges KE (2000) Ecology of snowshoe hares in southern boreal and montane forests. In: Ruggiero L, Aubry KB, Buskirk SW, Koehler GM, Krebs CJ, McKelvey KS, Squires JR (eds) Ecology and Conservation of Lynx in the United States. University Press of Colorado, Boulder p 163–206
Hoekstra HE (2006) Genetics, development and evolution of adaptive pigmentation in vertebrates. Heredity 97:222–234
pubmed: 16823403
Hoekstra HE, Krenz JG, Nachman MW (2005) Local adaptation in the rock pocket mouse (Chaetodipus intermedius): natural selection and phylogenetic history of populations. Heredity 94:217–228
pubmed: 15523507
Hoekstra HE, Nachman MW (2003) Different genes underlie adaptive melanism in different populations of rock pocket mice. Mol Ecol 12:1185–1194
pubmed: 12694282
Hubbard JK, Uy JAC, Hauber ME, Hoekstra HE, Safran RJ (2010) Vertebrate pigmentation: from underlying genes to adaptive function. Trends Genet 26:231–239
pubmed: 20381892
Jensen JD (2014) On the unfounded enthusiasm for soft selective sweeps. Nat Commun 5:5281
pubmed: 25345443
Jensen JD, Payseur BA, Stephan W, Aquadro CF, Lynch M, Charlesworth D, Charlesworth B (2019) The importance of the Neutral Theory in 1968 and 50 years on: a response to Kern & Hahn 2018. Evolution 73:111–4
pubmed: 30460993
Jones MR, Mills LS, Alves PC, Callahan CM, Alves JM, Lafferty DJR et al. (2018) Adaptive introgression underlies polymorphic seasonal camouflage in snowshoe hares. Science 360:1355–1358
pubmed: 29930138
Kettlewell HBD (1955) Selection experiments on industrial melanism in the Lepidoptera. Heredity 9:323–342
Kim Y, Nielsen R (2004) Linkage disequilibrium as a signature of selective sweeps. Genetics 167:1513–1524
pmcid: 1470945
pubmed: 15280259
Lande R, Shannon S (1996) The role of genetic variation in adaptation and population persistence in a changing environment. Evolution 50:434–437
pubmed: 28568879
Laurent S, Pfeifer SP, Settles ML, Hunter SS, Hardwick KM, Ormond L et al. (2016) The population genomics of rapid adaptation: disentangling signatures of selection and demography in white sands lizards. Mol Ecol 25:306–323
pubmed: 26363411
Lenormand T (2002) Gene flow and the limits to natural selection. Trends Ecol Evol 17:183–189
Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760
pmcid: 2705234
pubmed: 19451168
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N et al(2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25:2078–2079
pmcid: 19505943
pubmed: 19505943
Linnen CR, Kingsley EP, Jensen JD, Hoekstra HE (2009) On the origin and spread of an adaptive allele in deer mice. Science 325:1095–1098
pmcid: 2736094
pubmed: 2736094
Linnen CR, O’Quin CT, Shackleford T, Lindstedt C (2018) Genetic basis of body color and spotting pattern in redheaded pine sawfly larvae (Neodiprion lecontei). Genetics 209:291–305
pmcid: 5937194
pubmed: 5937194
Linnen CR, Poh YP, Peterson BK, Barrett RDH, Larson JG, Jensen JD, Hoekstra HE (2013) Adaptive evolution of multiple traits through multiple mutations at a single gene. Science 339:1312–1316
Lunter G, Goodson M (2011) Stampy: a statistical algorithm for sensitive and fast mapping of Illumina sequence reads. Genome Res 21:936–939
pmcid: 3106326
pubmed: 3106326
Majerus MEN (1998) Melanism: evolution in action. Oxford University Press, Oxford
Mallarino R, Linden TA, Linnen CR, Hoekstra HE (2017) The role of isoforms in the evolution of cryptic coloration in Peromyscus mice. Mol Ecol 26:245–258
McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A et al. (2010) The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20:1297–1303
pmcid: 2928508
pubmed: 20644199
Meirmans PG (2015) Seven common mistakes in population genetics and how to avoid them. Mol Ecol 24:3223–3231
pubmed: 25974103
Melo-Ferreira J, Seixas FA, Cheng E, Mills LS, Alves PC (2014) The hidden history of the snowshoe hare, Lepus americanus: extensive mitochondrial DNA introgression inferred from multilocus genetic variation. Mol Ecol 23:4617–4630
pubmed: 25113393
Merkin J, Russell C, Chen P, Burge CB (2012) Evolutionary dynamics of gene and isoform regulation in Mammalian tissues. Science 338:1593–1599
pmcid: 3568499
pubmed: 23258891
Mills LS, Bragina VE, Kumar AV, Zimova M, Lafferty DJR, Feltner J et al. (2018) Winter coat color polymorphisms identify global hotspots for evolutionary rescue from climate change. Science 359:1033–1036
pubmed: 29449510
Nachman MW, Hoekstra HE, D’Agostino SL (2003) The genetic basis of adaptive melanism in pocket mice. Proc Natl Acad Sci USA 100:5268–5273
Nadeau NJ, Pardo-Diaz C, Whibley A, Supple MA, Saenko SV, Wallbank RWR et al. (2016) The gene cortex controls mimicry and crypsis in butterflies and moths. Nature 534:106–110
pmcid: 5094491
pubmed: 5094491
Nielsen R, Williamson S, Kim Y, Hubisz MJ, Clark AG, Bustamante C (2005) Genomic scans for selective sweeps using SNP data. Genome Res 15:1566–1575
pmcid: 1310644
pubmed: 1310644
Orr HA (2010) The population genetics of beneficial mutations. Philos Trans R Soc Lond B Biol Sci 365:1195–1201
pmcid: 2871816
pubmed: 2871816
Orr HA, Betancourt AJ (2001) Haldane’s sieve and adaptation from the standing genetic variation. Genetics 157:875–884
pmcid: 1461537
pubmed: 1461537
Pavlidis P, Alachiotis N (2017) A survey of methods and tools to detect recent and strong positive selection. J Biol Res-Thessalon 24:7
pmcid: 5385031
pubmed: 5385031
Pavlidis P, Zivkovic D, Stamatakis A, Alachiotis N (2013) SweeD: likelihood-based detection of selective sweeps in thousands of genomes. Mol Biol Evol 30:2224–2234
pmcid: 3748355
pubmed: 3748355
Pfeifer SP (2017) From next-generation resequencing reads to a high-quality variant data set. Heredity 118:111–124
Pfeifer SP, Laurent S, Sousa VC, Linnen CR, Foll M, Excoffier L et al. (2018) The evolutionary history of Nebraska deer mice: local adaptation in the face of strong gene flow. Mol Biol Evol 35:792–806
pmcid: 5905656
pubmed: 5905656
Pfennig K, Kelly AL, Piece AA (2016) Hybridization as a facilitator of species range expansion. Proc Camb Philos Soc 283:20161329
Poh YP, Domingues VS, Hoekstra HE, Jensen JD (2014) On the prospect of identifying adaptive loci in recently bottlenecked populations. PLoS ONE 9:e110579
pmcid: 4226487
pubmed: 25383711
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
pmcid: 1461096
pubmed: 1461096
Ralph P, Coop G (2010) Parallel adaptation: one or many waves of advance of an advantageous allele? Genetics 186:647–668
pmcid: 2954473
pubmed: 20660645
Ralph PL, Coop G (2015) Convergent evolution during local adaptation to patchy landscapes. PLoS Genet 11:e1005630
pmcid: 4646681
pubmed: 26571125
Rimmer A, Phan H, Mathieson I, Iqbal Z, Twigg SR, Wilkie AO et al. (2014) Integrating mapping-, assembly- and haplotype-based approaches for calling variants in clinical sequencing applications. Nat Genet 46:912–918
pmcid: 4753679
pubmed: 25017105
Rosenblum EB, Hoekstra HE, Nachman MW (2004) Adaptive reptile color variation and the evolution of the Mc1r gene. Evolution 58:1794–1808
pubmed: 15446431
Rosenblum EB, Römpler H, Schöneberg T, Hoekstra HE (2010) Molecular and functional basis of phenotypic convergence in white lizards at White Sands. Proc Natl Acad Sci USA 107:2113–2117
pubmed: 20080544
Rosenblum EB, Parent CE, Diepeveen ET, Noss C, Bi K (2017) Convergent phenotypic evolution despite contrasting demographic histories in the fauna of White Sands. Am Nat 190:S44–S56
pubmed: 28731825
Sedlazeck FJ, Rescheneder F, von Haeseler A (2013) NextGenMap: fast and accurate read mapping in highly polymorphic genomes. Bioinformatics 29:2790–2791
pubmed: 23975764
Steiner CC, Römpler H, Boettger LM, Schöneberg T, Hoekstra HE (2009) The genetic basis of phenotypic convergence in beach mice: similar pigment patterns but different genes. Mol Biol Evol 26:35–45
pubmed: 18832078
Steiner CC, Weber JN, Hoekstra HE (2007) Adaptive variation in beach mice produced by two interacting pigmentation genes. PLoS Biol 5:e219
pmcid: 1945039
pubmed: 17696646
Stern DL, Orgogozo V (2008) The loci of evolution: how predictable is genetic evolution? Evolution 62:2155–2177
pmcid: 2613234
pubmed: 18616572
Teshima KM, Przeworski M (2006) Directional positive selection on an allele of arbitrary dominance. Genetics 172:713–718
pmcid: 1456198
pubmed: 16219788
Tigano A, Friesen VL (2016) Genomics of local adaptation with gene flow. Mol Ecol 25:2144–2164
pubmed: 26946320
Thornton KR, Jensen JD (2007) Controlling the false-positive rate in multilocus genome scans for selection. Genetics 175:737–750
pmcid: 1800626
pubmed: 17110489
Vignieri SN, Larson JG, Hoekstra HE (2010) The selective advantage of crypsis in mice. Evolution 64:2153–2158
pubmed: 20163447
Vrieling H, Duhl DM, Millar SE, Miller KA, Barsh GS (1994) Differences in dorsal and ventral pigmentation result from regional expression of the mouse agouti gene. Proc Natl Acad Sci USA 91:5667–5671
pubmed: 8202545
Yassin A, Bastide H, Chung H, Veuille M, David JR, Pool JE (2016) Ancient balancing selection at tan underlies female colour dimorphism in Drosophila erecta. Nat Commun 7:10400
pmcid: 4735637
pubmed: 26778363
Yeaman S, Whitlock MC (2011) The genetic architecture of adaptation under migration-selection balance. Evolution 65:1897–1911
pubmed: 21729046
Zimova M, Mills LS, Nowak JJ (2016) High fitness costs of climate change-induced camouflage mismatch. Ecol Lett 19:299–307