Abstract
Callicarpa subpubescens, endemic to the Ogasawara Islands, is suggested to have multiple ecotypes in the Hahajima Islands, specifically in the central part of the Ogasawara Islands. In this study, associations between genetic groups and spatial distribution, habitat, leaf morphology, size structure, and flowering time of each genetic group were investigated on Hahajima and the satellite Imoutojima Islands. Genetic groups were identified using EST-SSR markers, revealing four ecotypes named based on morphological features: Dwarf (D), Glabrescent (G), Tall (T), and Middle (M), with M being a result of the hybridization of G and T. Ecotype D, adapted to dry environments, is characterized by small tree size, dense thick leaves with abundant hairs, and is distributed in dry scrub. Ecotype G, adapted to understory of mesic forests, lacks leaf hairs. Ecotype T, adapted to the canopy of mesic forests, has hairy leaves and is tall in tree height. Ecotype M, adapted to the canopy of mesic scrub or edges of mesic forests, has hairy leaves but with a shorter tree height than ecotype T. Flowering peaks differed among all ecotype pairs except G and M, but the flowering times more or less overlapped among all ecotypes, suggesting that pre-mating isolation among ecotypes is not perfect. Post-mating isolation is considered absent, as there were no differences in the results, germination, and survival rates of one-year seedlings among inter- and intra-ecotype crossings. The existence of such ecotypes provides valuable insights into the ongoing speciation processes adapting to the oceanic island environments.
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Data availability
The data supporting the findings of this study are available from Dryad https://doi.org/10.5061/dryad.6q573n65w.
References
Abe T (2006) Threatened pollination systems in native flora of the Ogasawara (Bonin) Islands. Ann Bot 98(2):317–334
Adams WT (1992) Gene dispersal within forest tree populations. New For 6(1):217–240
Arnold ML, Hodges SA (1995) Are natural hybrids fit or unfit relative to their parents? Trends Ecol Evol 10(2):67–71
Arnold ML, Kunte K (2017) Adaptive genetic exchange: A tangled history of admixture and evolutionary innovation. Trends Ecol Evol 32(8):601–611
Baldwin BG (1997) Adaptive radiation of the Hawaiian silversword alliance: Congruence and conflict of phylogenetic evidence from molecular and non-molecular investigations. In: Givnish TJ, Sytsma KJ (eds) Molecular Evolution and Adaptive Radiation. Cambridge University Press, New York, pp 103–128
Barton NH (2001) The role of hybridization in evolution. Mol Ecol 10(3):551–568
Barton NH, Hewitt GM (1985) Analysis of Hybrid Zones. Annu Rev Ecol Syst 16:113–148
Biodiversity Center of Japan NCB, Ministry of the Environment. (1999-) Natural Environmental Information GIS, Vegetation survey (6th~). https://www.biodic.go.jp/trialSystem/EN/info/vg67.html
Bradshaw HD, Schemske DW (2003) Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers. Nature 426(6963):176–178
Burke JM, Arnold ML (2001) Genetics and the fitness of hybrids. Annu Rev Genet 35:31–52
Case AL, Willis JH (2008) Hybrid male sterility in Mimulus (Phrymaceae) is associated with a geographically restricted mitochondrial rearrangement. Evolution 62(5):1026–1039
Chhatre VE, Evans LM, DiFazio SP, Keller SR (2018) Adaptive introgression and maintenance of a trispecies hybrid complex in range-edge populations of Populus. Mol Ecol 27(23):4820–4838
Chiba S, Cowie RH (2016) Evolution and Extinction of Land Snails on Oceanic Islands. Annu Rev Ecol Evol Syst 47(1):123–141
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14(8):2611–2620
Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7(4):574–578
Foll M (2012) BayeScan v2. 1 User manual. Ecology 20:1450–1462
Gillespie RG, Howarth FG, Roderick GK (2001) Adaptive radiation. In: Levin SA (ed), Encyclopedia of biodiversity 1. Academic Press, New York, pp 25-44
Givnish T (1997) Adaptive radiation and molecular systematics: issues and approaches. Cambridge University Press, Cambridge
Grant BR, Grant PR (1996) High survival of Darwin’s finch hybrids: Effects of beak morphology and diets. Ecology 77(2):500–509
Gustafsson S, Lönn M (2003) Genetic differentiation and habitat preference of flowering-time variants within Gymnadenia conopsea. Heredity (Edinb) 91(3):284–292
Hoballah ME, Gübitz T, Stuurman J, Broger L, Barone M, Mandel T et al. (2007) Single gene–mediated shift in pollinator attraction in Petunia. Plant Cell 19(3):779–790
Ilyas M, Nisar M, Khan N, Hazrat A, Khan AH, Hayat K et al. (2021) Drought tolerance strategies in plants: A mechanistic approach. J Plant Growth Regul 40(3):926–944
Japan Meteorological Agency (2014) Past Weather Data of Japan. https://www.data.jma.go.jp/stats/etrn/index.php. Accessed 25 March 2024
Kato S, Matsumoto A, Yoshimura K, Katsuki T, Iwamoto K, Kawahara T et al. (2014) Origins of Japanese flowering cherry (Prunus subgenus Cerasus) cultivars revealed using nuclear SSR markers. Tree Genet Genomes 10(3):477–487
Kawakubo N (1986) Morphological variation of three endemic species of Callicarpa (Verbenaceae) in the Bonin (Ogasawara) Islands. Plant Species Biol 1:59–68
Kawakubo N (1990) Dioecism of the genus Callicarpa (Verbenaceae) in the Bonin (Ogasawara) Islands. botanical Mag= Shokubutsu-gaku-zasshi 103(1):57–66
Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I (2015) Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour 15(5):1179–1191
Lawson DJ, van Dorp L, Falush D (2018) A tutorial on how not to over-interpret STRUCTURE and ADMIXTURE bar plots. Nat Commun 9(1):3258
Lexer C, Welch ME, Durphy JL, Rieseberg LH (2003) Natural selection for salt tolerance quantitative trait loci (QTLs) in wild sunflower hybrids: implications for the origin of Helianthus paradoxus, a diploid hybrid species. Mol Ecol 12(5):1225–1235
Li X, Wei G, El-Kassaby YA, Fang Y (2021) Hybridization and introgression in sympatric and allopatric populations of four oak species. BMC Plant Biol 21(1):266
Loope L, Giambelluca T (1998) Vulnerability of island tropical montane cloud forests to climate change, with special reference to East Maui, Hawaii. Clim Change 39:503–517
Martin NH, Bouck AC, Arnold ML (2007) The genetic architecture of reproductive isolation in Louisiana irises: flowering phenology. Genetics 175(4):1803–1812
McGregor IR, Helcoski R, Kunert N, Tepley AJ, Gonzalez-Akre EB, Herrmann V et al. (2021) Tree height and leaf drought tolerance traits shape growth responses across droughts in a temperate broadleaf forest. New Phytol 231(2):601–616
Meier JI, Marques DA, Mwaiko S, Wagner CE, Excoffier L, Seehausen O (2017) Ancient hybridization fuels rapid cichlid fish adaptive radiations. Nat Commun 8(1):14363
Meirmans PG (2019) Subsampling reveals that unbalanced sampling affects Structure results in a multi-species dataset. Heredity (Edinb) 122(3):276–287
Ogasawara Environmental Planning Laboratory (2023) Ogasawara National Park, Hahajima Shinyuhigaoka Natural Restoration Zone Conservation Survey Activities Report, 2022. Kanto Regional Environmental Office, Ministry of the Environment (ed.): Saitama, Japan (in Japanese)
Okamoto T, Okuyama Y, Goto R, Tokoro M, Kato M (2015) Parallel chemical switches underlying pollinator isolation in Asian Mitella. J Evol Biol 28(3):590–600
Ono M (1991) The Flora of the Bonin (Ogasawara) Islands. Aliso 13(1):95–105
Ono M, Kobayashi S, Kawakubo N (1986) Present situation of endangered plant species in the Bonin Islands. Ogasawara Research 12:1–32
Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28(19):2537–2539
Pritchard JK, Stephens M, Donnelly PJ (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution: 1280–1283
Ripley BS, Pammenter NW, Smith VR (1999) Function of leaf hairs revisited: The hair layer on leaves Arctotheca populifolia reduces photoinhibition, but leads to higher leaf temperatures caused by lower transpiration rates. J Plant Physiol 155(1):78–85
Rousset F (2008) genepop’007: a complete re‐implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8(1):103–106
Rundle HD, Nosil P (2005) Ecological speciation. Ecol Lett 8(3):336–352
Sandstedt GD, Wu CA, Sweigart AL (2021) Evolution of multiple postzygotic barriers between species of the Mimulus tilingii complex. Evolution 75(3):600–613
Schluter D (2000) The ecology of adaptive radiation. Oxford Universiity Press, Oxford
Schluter D (2001) Ecology and the origin of species. Trends Ecol Evol 16(7):372–380
Seehausen O (2004) Hybridization and adaptive radiation. Trends Ecol Evol 19(4):198–207
Seehausen O, Takimoto G, Roy D, Jokela J (2008) Speciation reversal and biodiversity dynamics with hybridization in changing environments. Mol Ecol 17(1):30–44
Setsuko S, Narita S, Tamaki I, Sugai K, Nagano A-J, Ujino-Ihara T et al. (2023) Adaptive radiation of the Callicarpa genus in the Bonin Islands revealed through double-digest restriction site–associated DNA sequencing analysis. Authorea https://doi.org/10.22541/au.169865467.72711081/v1
Setsuko S, Sugai K, Uchiyama K, Katoh S, Kato H, Narita S et al. (2018) Development of microsatellite markers for Callicarpa subpubescens (Lamiaceae), an endemic species of the Bonin Islands. J Res 23(6):393–397
Shimizu Y (1992) Origin of Distylium dry forest and occurrence of endangered species in the Bonin Islands. Pac Sci 46(2):179–196
Shimizu Y (2001) Current status and regeneration pattern of Dendrocacalia crepidifolia on the Hahajima Island, Ogasawara Islands, Japan. Komazawa. Geography 37:17–36. (in Japanese)
Stanton ML, Galen C, Shore J (1997) Population structure along a steep environmental gradient: Consequences of flowering time and habitat variation in the snow buttercup, Ranunculus Adoneus. Evolution 51(1):79–94
Suarez-Gonzalez A, Hefer CA, Christe C, Corea O, Lexer C, Cronk QC et al. (2016) Genomic and functional approaches reveal a case of adaptive introgression from Populus balsamifera (balsam poplar) in P. trichocarpa (black cottonwood). Mol Ecol 25(11):2427–2442
Suarez-Gonzalez A, Lexer C, Cronk QCB (2018) Adaptive introgression: a plant perspective. Biol Lett 14(3)
Sugai K, Mori K, Murakami N, Kato H (2019) Strong genetic structure revealed by microsatellite variation in Callicarpa species endemic to the Bonin (Ogasawara) Islands J Plant Res 132(6):759–775
Sugai K, Setsuko S, Nagamitsu T, Murakami N, Kato H, Yoshimaru H (2022) Environmental and genetic effects on phenotypic differences between Elaeocarpus photiniifolia (Elaeocarpaceae) ecotypes in dry and mesic habitats on a Japanese oceanic island. Plant Species Biol 38:67–78
Todesco M, Pascual MA, Owens GL, Ostevik KL, Moyers BT, Hübner S et al. (2016) Hybridization and extinction. Evol Appl 9(7):892–908
Tomiyama K, Kurozumi T (1991) Living condition and conservation of land snails in the Ogasawara Islands. In: Ono M, Kimura M, Miyasita K, Nogami M (eds) Report of the second general survey of natural environment of the Ogasawara Islands. Tokyo Metropolitan Office, Tokyo, pp 245–281 (in Japanese)
Tsujii Y, Onoda Y, Izuno A, Isagi Y, Kitayama K (2016) A quantitative analysis of phenotypic variations of Metrosideros polymorpha within and across populations along environmental gradients on Mauna Loa, Hawaii. Oecologia 180(4):1049–1059
Tsuneki S, Kato H, Murakami N (2014) Ecological and genetic differentiation in Persea boninensis (Lauraceae) endemic to the Bonin (Ogasawara) Islands. Plant Species Biol 29(1):16–24
Turesson G (1922a) The species and the variety as ecological units. Hereditas 3(1):100–113
Turesson G (1922b) The genotypical response of the plant species to the habitat. Hereditas 3(3):211–350
Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4(3):535–538
Yang C-F, Gituru RW, Guo Y-H (2007) Reproductive isolation of two sympatric louseworts, Pedicularis rhinanthoides and Pedicularis longiflora (Orobanchaceae): how does the same pollinator type avoid interspecific pollen transfer? Biol J Linn Soc 90(1):37–48
Yelmen B, Marnetto D, Molinaro L, Flores R, Mondal M, Pagani L (2021) Improving delection detection with population branch statistic on admixed populations. Genome Biol Evol 13(4). https://doi.org/10.1093/gbe/evab039
Acknowledgements
The authors are grateful to Y. Nakamura for providing the location of trees; Dr. C. Migita, A. Hisamatsu, M. Yokoya and Y. Yoshii for their experimental support; Drs. T. Nagamitsu and J.R.P. Worth for their valuable advice. We also thank Metropolis of Tokyo, the Ministry of the Environmental Government of Japan, and Forestry Agency of Japan for allowing this study. This research was conducted using the Ogasawara Field Research Station of Tokyo Metropolitan University. This work was funded by Grants-in-Aid for Science Research from the Japanese Society for Promotion of Science (JP26290073, JP15K07203, JP21K05694), the Environment Research and Technology Development Fund of the Ministry of the Environment, Japan (4-1402).
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SS, KS, KH, and HK designed the research. SS, KS, KH, and HK sampled materials. SS performed all the laboratory work. SS, KS, and IT performed data analysis. All co-authors discussed the results. SS and IT wrote the paper.
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The plant species sampled for this study were obtained within the Ogasawara National Park, and sampling was conducted with permission from the Ministry of the Environment, the Forestry Agency of Japan, and the Tokyo Metropolitan Government.
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Setsuko, S., Sugai, K., Tamaki, I. et al. Ecotype variation in the endemic tree Callicarpa subpubescens on small oceanic islands: genetic, phenotypic, and environmental insights. Heredity (2024). https://doi.org/10.1038/s41437-024-00684-3
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DOI: https://doi.org/10.1038/s41437-024-00684-3