Range shift and introgression of the rear and leading populations in two ecologically distinct Rubus species

BMC Evolutionary Biology

Tetsukazu Yahara³  Martin Lascoux²  Misako Mishima¹  Makiko Mimura⁴ 

[1] The Kyushu University Museum, 6-10-1 Hakozaki, Higashi-ku 812-8581, Fukuoka, Japan;Centre for Computational Systems Biology, Fudan University, 220 Handan Road, Shanghai 200433, PRC, China;Department of Biology, Kyushu University, 6-10-1 Hakozaki, Higashi-ku 812-8581, Fukuoka, Japan;Current address: Tamagawa University, 6-1-1 Tamagawa-Gakuen, Machida, Tokyo, Japan

关键词: Climate change;    Isolation with migration;    Phylogeography;    Colonizer;    Introgression;    Species boundaries;   

Others  :  1117871
DOI  :  10.1186/s12862-014-0209-9

 received in 2014-05-05, accepted in 2014-09-23,  发布年份 2014

【 摘 要 】

Background

The margins of a species’ range might be located at the margins of a species’ niche, and in such cases, can be highly vulnerable to climate changes. They, however, may also undergo significant evolutionary changes due to drastic population dynamics in response to climate changes, which may increase the chances of isolation and contact among species. Such species interactions induced by climate changes could then regulate or facilitate further responses to climatic changes. We hypothesized that climate changes lead to species contacts and subsequent genetic exchanges due to differences in population dynamics at the species boundaries. We sampled two closely related Rubus species, one temperate (Rubus palmatus) and the other subtropical (R. grayanus) near their joint species boundaries in southern Japan. Coalescent analysis, based on molecular data and ecological niche modelling during the Last Glacial Maximum (LGM), were used to infer past population dynamics. At the contact zones on Yakushima (Yaku Island), where the two species are parapatrically distributed, we tested hybridization along altitudinal gradients.

Results

Coalescent analysis suggested that the southernmost populations of R. palmatus predated the LGM (~20,000 ya). Conversely, populations at the current northern limit of R. grayanus diverged relatively recently and likely represent young outposts of a northbound range shift. These population dynamics were partly supported by the ensemble forecasting of six different species distribution models. Both past and ongoing hybridizations were detected near and on Yakushima. Backcrosses and advanced-generation hybrids likely generated the clinal hybrid zones along altitudinal gradients on the island where the two species are currently parapatrically distributed.

Conclusions

Climate oscillations during the Quaternary Period and the response of a species in range shifts likely led to repeated contacts with the gene pools of ecologically distinct relatives. Such species interactions, induced by climate changes, may bring new genetic material to the marginal populations where species tend to experience more extreme climatic conditions at the margins of the species distribution.

【 授权许可】

   
2014 Mimura et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

【 参考文献 】

• [1]Brown JH: On the relationship between abundance and distribution of species. Am Nat 1984, 124:255-279.
• [2]Eckert CG, Samis KE, Lougheed SC: Genetic variation across species’ geographical ranges: the central–marginal hypothesis and beyond. Mol Ecol 2008, 17:1170-1188.
• [3]Lesica P, Allendorf FW: When are peripheral populations valuable for conservation? Conserv Biol 1995, 9:753-760.
• [4]Hewitt G: The genetic legacy of the Quaternary ice ages. Nature 2000, 405:907-913.
• [5]Davis MB, Shaw RG: Range shifts and adaptive responses to Quaternary climate change. Science 2001, 292:673-679.
• [6]Hampe A, Petit RJ: Conserving biodiversity under climate change: the rear edge matters. Ecol Lett 2005, 8:461-467.
• [7]Eo SH, Wares JP, Carroll JP: Population divergence in plant species reflects latitudinal biodiversity gradients. Biol Lett 2008, 4:382-384.
• [8]Seehausen O, TAkimoto G, Roy D, Jokela J: Speciation reversal and biodiversity dynamics with hybridization in changing environments. Mol Ecol 2008, 17:30-44.
• [9]Barton NH, Hewitt GM: Analysis of hybrid zones. Annu Rev Ecol Syst 1985, 16:113-148.
• [10]Arnold ML, Hodges SA: Are natural hybrids fit or unfit relative to their parents? Trends Ecol Evol 1995, 10:67-71.
• [11]Mallet J: Hybridization as an invasion of the genome. Trends Ecol Evol 2005, 20:229-237.
• [12]Whitney KD, Randell RA, Rieseberg LH: Adaptive introgression of herbivore resistance traits in the weedy sunflower Helianthus annuus. Am Nat 2006, 167:794-807.
• [13]Pardo-Diaz C, Salazar C, Baxter SW, Merot C, Figueiredo-Ready W, Joron M, McMillan WO, Jiggins CD: Adaptive introgression across species boundaries in Heliconius butterflies. PLoS Genet 2012, 8:e1002752.
• [14]Whitney KD, Randell RA, Rieseberg LH: Adaptive introgression of abiotic tolerance traits in the sunflower Helianthus annuus. New Phytol 2010, 187:230-239.
• [15]Martin NH, Bouck AC, Arnold ML: Detecting adaptive trait introgression between Iris fulva and I. brevicaulis in highly selective field conditions. Genetics 2006, 172:2481-2489.
• [16]Garroway CJ, Bowman J, Cascaden TJ, Holloway GL, Mahan CG, Malcolm JR, Steele MA, Turner G, Wilson PJ: Climate change induced hybridization in flying squirrels. Glob Change Biol 2010, 16:113-121.
• [17]Barton NH: The role of hybridization in evolution. Mol Ecol 2001, 10:551-568.
• [18]Donovan LA, Rosenthal DR, Sanchez-Velenosi M, Rieseberg LH, Ludwig F: Are hybrid species more fit than ancestral parent species in the current hybrid species habitats? J Evol Biol 2010, 23:805-816.
• [19]Tsukada M: Map of vegetation during the last glacial maximum in Japan. Quaternary Res 1985, 23:369-381.
• [20]Savolainen O, Pyhajarvi T: Genomic diversity in forest trees. Curr Opin Plant Biol 2007, 10:162-167.
• [21]Evanno G, Regnaut S, Goudet J: Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 2005, 14:2611-2620.
• [22]Pritchard JK, Stephens M, Donnelly P: Inference of population structure using multilocus genotype data. Genetics 2000, 155:945-959.
• [23]Thuiller W, Lafourcade B, Araujo M: The Presentation Manual for BIOMOD. Laboratoire d'Écologie Alpine, Université Joseph Fourier, Grenoble, France; 2012.
• [24]Schonswetter P, Paun O, Tribsch A, Niklfeld H: Out of the Alps: colonization of Northern Europe by East Alpine populations of the glacier buttercup Ranunculus glacialis L. (Ranunculaceae). Mol Ecol 2003, 12:3373-3381.
• [25]Ehrich D, Alsos IG, Brochmann C: Where did the northern peatland species survive the dry glacials: cloudberry (Rubus chamaemorus) as an example. J Biogeogr 2008, 35:801-814.
• [26]Petit RJ, Aguinagalde I, de Beaulieu J-L, Bittkau C, Brewer S, Cheddadi R, Ennos R, Fineschi S, Grivet D, Lascoux M: Glacial refugia: hotspots but not melting pots of genetic diversity. Science 2003, 300:1563-1565.
• [27]Aoki K, Suzuki T, Murakami N, Hsu T-W: Phylogeography of the component species of broad-leaved evergreen forests in Japan, based on chloroplast DNA variation. J Plant Res 2004, 117:77-94.
• [28]Yahara T, Ohba H, Murata J, Iwatsuki K: Taxonomic review of vascular plants endemic to Yakushima Island. Japan J Fac Sci Univ Tokyo III 1987, 14:69-119.
• [29]Jordano P: Seed weight variation and differential avian dispersal in blackberries Rubus ulmifolius. Oikos 1984, 43:149-153.
• [30]Traveset A, Willson MF: Ecology of the fruit-colour polymorphism in Rubus spectabilis. Evol Ecol 1998, 12:331-345.
• [31]Jordano P: Migrant birds are the main seed dispersers of blackberries in southern Spain. Oikos 1982, 38:183-193.
• [32]Strasburg JL, Rieseberg LH: How robust are “isolation with migration” analyses to violations of the IM model? A simulation study. Mol Biol Evol 2010, 27:297-310.
• [33]Melo-Ferreira J, Boursot P, Suchentrunk F, Ferrand N, Alves PC: Invasion from the cold past: extensive introgression of mountain hare (Lepus timidus) mitochondrial DNA into three other hare species in northern Iberia. Mol Ecol 2005, 14:2459-2464.
• [34]Rieseberg LH, Kim S-C, Randell RA, Whitney KD, Gross BL, Lexer C, Clay K: Hybridization and the colonization of novel habitats by annual sunflowers. Genetica 2007, 129:149-165.
• [35]Rieseberg LH, Blackman BK: Speciation genes in plants. Ann Bot 2010, 106:439-455.
• [36]Anderson E: Hybridization of the habitat. Evolution 1948, 2:1-9.
• [37]Rieseberg LH: Hybrid origins of plant species. Annu Rev Ecol Syst 1997, 28:359-389.
• [38]Excoffier L, Ray N: Surfing during population expansions promotes genetic revolutions and structuration. Trends Ecol Evol 2008, 23:347-351.
• [39]Guichoux E, Garnier-Géré P, Lagache L, Lang T, Boury C, Petit RJ: Outlier loci highlight the direction of introgression in oaks. Mol Ecol 2013, 22:450-462.
• [40]Haygood R, Ives AR, Andow DA: Consequences of recurrent gene flow from crops to wild relatives. Proc R Soc B-Biol Sci 2003, 270:1879-1886.
• [41]Currat M, Ruedi M, Petit RJ, Excoffier L: The hidden side of invasions: massive introgression by local genes. Evolution 2008, 62:1908-1920.
• [42]Lexer C, Joseph JA, van Loo M, Barbara T, Heinze B, Bartha D, Castiglione S, Fay MF, Buerkle CA: Genomic admixture analysis in European Populus spp. reveals unexpected patterns of reproductive isolation and mating. Genetics 2010, 186:699-712.
• [43]Ingvarsson PK, García MV, Hall D, Luquez V, Jansson S: Clinal variation in phyB2, a candidate gene for day-length-induced growth cessation and bud set, across a latitudinal gradient in European aspen (Populus tremula). Genetics 2006, 172:1845-1853.
• [44]Ingvarsson PK, Garcia MV, Luquez V, Hall D, Jansson S: Nucleotide polymorphism and phenotypic associations within and around the phytochrome B2 locus in European aspen (Populus tremula, Salicaceae). Genetics 2008, 178:2217-2226.
• [45]Hedrick PW: Adaptive introgression in animals: examples and comparison to new mutation and standing variation as sources of adaptive variation. Mol Ecol 2013, 22:4606-4618.
• [46]Castric V, Bechsgaard J, Schierup MH, Vekemans X: Repeated adaptive introgression at a gene under multiallelic balancing selection. PLoS Genet 2008, 4:e1000168.
• [47]Arnold ML, Martin NH: Adaptation by introgression. J Biol 2009, 8:82. BioMed Central Full Text
• [48]Rieseberg L: Adaptive introgression: the seeds of resistance. Curr Biol 2011, 21:R581-R583.
• [49]Song Y, Endepols S, Klemann N, Richter D, Matuschka F-R, Shih C-H, Nachman MW, Kohn MH: Adaptive introgression of anticoagulant rodent poison resistance by hybridization between Old World mice. Curr Biol 2011, 21:1296-1301.
• [50]Rozen S, Skaletsky H: Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 2000, 132:365-386.
• [51]Doyle J: DNA protocols for plants. In Molecular techniques in taxonomy NATO ASI Series. Volume 57. Edited by Hewitt GM, Johnston AWB, Young JPW. Springer, New York; 1991:283-293.
• [52]Stephens M, Smith NJ, Donnelly P: A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 2001, 68:978-989.
• [53]Nei M: Molecular evolutionary genetics. Columbia University Press, New York; 1987.
• [54]Hudson RR, Kreitman M, Aguadé M: A test of neutral molecular evolution based on nucleotide data. Genetics 1987, 116:153-159.
• [55]Wright SI, Charlesworth B: The HKA test revisited: a maximum-likelihood-ratio test of the standard neutral model. Genetics 2004, 168:1071-1076.
• [56]Tajima F: The effect of change in population size on DNA polymorphism. Genetics 1989, 123:597-601.
• [57]Fu YX, Li WH: Statistical tests of neutrality of mutations. Genetics 1993, 133:693-709.
• [58]Hey J, Nielsen R: Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 2004, 167:747-760.
• [59]Hey J: Isolation with migration models for more than two populations. Mol Biol Evol 2010, 27:905-920.
• [60]Koch MA, Haubold B, Mitchell-Olds T: Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). Mol Biol Evol 2000, 17:1483-1498.
• [61]Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen GL, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, et al.: The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 2006, 313:1596-1604.
• [62]Gompert Z, Buerkle CA: Introgress: a software package for mapping components of isolation in hybrids. Mol Ecol Resour 2010, 10:378-384.
• [63]Hamilton JA, Lexer C, Aitken SN: Genomic and phenotypic architecture of a spruce hybrid zone (Picea sitchensis × P. glauca). Mol Ecol 2013, 22:827-841.
• [64]Anderson EC, Thompson EA: A model-based method for identifying species hybrids using multilocus genetic data. Genetics 2002, 160:1217-1229.
• [65]Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A: Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 2005, 25:1965-1978.
• [66]Elith J, Graham CH, Anderson RP, Dudík M, Ferrier S, Guisan A, Hijmans RJ, Huettmann F, Leathwick JR, Lehmann A, Li J, Lohmann LG, Loiselle BJ, Manion G, Moritz C, Nakamura M, Nakazawa Y, Overton JM, Peterson AT, Phillips SJ, Richardson K, Scachetti-Pereira R, Schapire RE, Soberon J, Williams S, Wisz MS, Zimmermann NE: Novel methods improve prediction of species’ distributions from occurrence data. Ecography 2006, 29:129-151.
• [67]Thuiller W, Lafourcade B, Engler R, Araújo MB: BIOMOD - a platform for ensemble forecasting of species distributions. Ecography 2009, 32:369-373.
• [68]Thuiller W: BIOMOD–optimizing predictions of species distributions and projecting potential future shifts under global change. Glob Change Biol 2003, 9:1353-1362.
• [69][http://www.R-project.org/] webcite R Core Team: R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2014. .
• [70]Barbet-Massin M, Jiguet F, Cécile Albert H, Thuiller W: Selecting Pseudo-Absences for Species Distribution Models: How, Where and How Many? Methods in Ecology and Evolution 2012, 3:327-38.
• [71]Phillips SJ, Anderson RP, Schapire RE: Maximum entropy modeling of species geographic distributions. Ecol Model 2006, 190:231-259.