Mayr (1963)提出的異域種化模式是指兩族群因地理障礙的產生，造成族群分化且分化後將不再有基因交流(gene flow)，海洋性島嶼的生物起源便被廣泛認為是異域種化(allopatric speciation)的經典例子。然而，大陸性島嶼物種的種化過程可能較為複雜；過去冰河週期時，大陸性島嶼與鄰近大陸因海平面的上升下降，經歷週期性的相連，此連結為原本分隔的族群提供了基因交流的機會。因此，Mayr(1963)提出的異域種化模式可能並不完全適用於解釋大陸性島嶼物種的起源。本研究以畫眉(Garrulax canorus)及其姊妹種台灣畫眉(G. taewanus)為例子，採用“isolation with migration model”估算兩物種的分化時間、分化後的基因交流頻率、兩物種的有效族群量及祖先族群量。畫眉分佈於東亞大陸東南部及中南半島北部，而台灣畫眉則僅分佈於台灣。本研究選取10個核DNA片段，其中包含3個核基因內含子(nuclear intron)和7個基因體中位置未知的核片段（共3958bp），分別對兩種畫眉進行定序及族群遺傳參數的估算。結果顯示，兩種畫眉於3.3百萬年前開始分化，此分化時間明顯的早於依據粒線體DNA序列所推估出來的分化時間(1.5百萬年)。基因交流頻率方面，畫眉播遷至台灣的基因交流頻率明顯不等於零(mGt = 0.88、2NGtmGt = 0.12)，而反方向的播遷則明顯較低(mGc = 0.06、2NGcmGc = 0.048)。因此兩種畫眉在分化後有不對稱的基因交流現象。依據結果，我們提出兩種可能種化的過程：第一，兩種畫眉是在異域（如海水屏障或棲地不相連）的情況下開始分化，而在陸地相連時兩族群發生基因交流。第二，在並域(parapatry)的狀況下，兩族群可能因天擇壓力不同或族群高度結構化，造成分化。無論是上述何種機制，皆顯示畫眉種化過程不符合傳統的異域種化模式。此研究提供了一個檢測異域種化的範例且對大陸性島嶼的物種起源機制提出了新的觀點。

The origins of endemic species on remote oceanic islands have been well explained by a strict allopatric speciation model as advocated by Mayr (1963). A strictly allopatric speciation model indicates that populations are isolated by a geographic barrier, and gene flow would cease completely after the barrier was formed. However, for species inhibiting continental islands, their speciation processes might be more complicated. In continental island systems, geographic barriers might not always exist during glacial episodes. These islands may periodically be connected to the adjacent continent at the lowstand of sea level during glacial periods. Therefore, the speciation mode for continental islands biota might not completely agree with the strictly allopatric speciation mode. In this study, we adopted an “isolation with migration” model to estimate divergence times, migration rates after splitting, and the effective population sizes of a pair of sister species, Hwamei (Garrulax canorus) and Taiwan Hwamei (G. taewanus) which are distributed on the Asian mainland and in Taiwan, respectively. We sequenced three nuclear introns and seven anonymous nuclear loci (with a total length of 3958 bp) to reveal that two hwamei species have diverged 3.3 million years ago which is earlier than the time estimated from mtDNA data (about 1.5 million years ago). Our results provided an unequivocal evidence of gene flow from G. canorus to G. taewanus (mGt = 0.88、2NGtmGt = 0.12) since their divergence. However, migration rate in the opposite direction was relatively low (mGc = 0.06、2NGcmGc = 0.048). We proposed two possible scenarios of speciation processes to explain the divergence with migration of two hwamei species. First, divergence of the two hwamei species was initiated allopatrically by the development of oceanic or other habitat barriers. However, gene flow periodically occurred when land bridges were exposed. Second, the divergence of the two hwamei species might be initiated parapatrically due to local selection or high levels of genetic structure between the populations. In conclusion, our results suggest that the divergence between hwameis does not fit a strictly allopatric speciation mode. Our results provided a good example to reject the strictly allopatric speciation paradigm and shed a new light on the origin of continental island biota.

Andersson, M. 1994. Sexual Selection. Princeton University Press, Princeton, NJ.
Avise, J. C., J. Arnold, R. M. Ball, E. Bermingham, T. Lamb, J. E. Neigel, C. A. Reeb, and N. C. Saunders. 1987. Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annual Review of Ecology and Systematics 18:489-522.
Axelsson, E., N. G. Smith, H. Sundstrom, S. Berlin, and H. Ellegren. 2004. Male-biased mutation rate and divergence in autosomal, z-linked and w-linked introns of chicken and turkey. Molecular Biology and Evolution 21:1538-1547.
Bandelt, H. J., P. Forster, and A. Röhl. 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16:37-48
Beebee, T. J. C. 2004. An Introduction to Molecular Ecology. Oxford University Press, New York.
Bossuyt, F., M. Meegaskumbura, N. Beenaerts, D. J. Gower, R. Pethiyagoda, K. Roelants, A. Mannaert, M. Wilkinson, M. M. Bahir, K. Manamendra-Arachchi, P. K. Ng, C. J. Schneider, O. V. Oommen, and M. C. Milinkovitch. 2004. Local endemism within the Western Ghats-Sri Lanka biodiversity hotspot. Science 306:479-481.
Brooker, L., M. Brooker, and P. Cale. 1999. Animal dispersal in fragmented habitat: measuring habitat connectivity, corridor use, and dispersal mortality. Conservation Ecology [online] 3:4. URL: http://www.consecol.org/vol3/
issl/art4.
Buonaccorsi, V., K. Reece, L. Morgan, and J. Graves. 1999. Geographic distribution of molecular variance within the blue marlin (Makaira nigricans): a hierarchical analysis of allozyme, single-copy nuclear, and mitochondrial DNA markers. Evolution 53:568-579.
Coyne, J. A., and H. A. Orr. 2004. Allopatric and parapatric speciation. 83-124. Speciation. Sinauer Associates, Sunderland, MA.
Darwin, C. 1859. On the Origin of Species. John Murray, London.
Eedler, J. A. 1977. Geographic variation, speciation and clines. Princeton University Press, New Jersey.
Gavrilets, S. 2000. Waiting time to parapatric speciation. Proceeding of the Royal Society of London B, Biological Sciences 267:2483-2492.
Gavrilets, S., H. Li, and M. D. Vose. 2000. Patterns of parapatric speciation. Evolution 54:1126-1134.
Gemmell, N. J., and S. Akiyama. 1996. An efficient method for the extraction of DNA from vertebrate tissues. Trends in Genetics 12:338-339.
Grant, P. R., and B. R. Grant. 1998. Speciation and hybridization of birds on islands. 142-162 in P. R. Grant, ed. Evolution on Islands. Oxford University Press, New York.
Hare, M. P., and J. C. Avise. 1998. Population structure in the American oyster as inferred by nuclear gene genealogies. Molecular Biology and Evolution 15:119-128.
Harrison, S. P., G. Yu, H. Takahara, and I. C. Prentice. 2001. Palaeovegetation. Diversity of temperate plants in East Asia. Nature 413:129-130.
Hasegawa, M., H. Kishino, and T. Yano. 1985. Dating of the human ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22:160-174.
Hey, J., and R. Nielsen. 2004. Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 167:747-760.
Hey, J., and R. Nielsen. 2005. IM - A program for fitting the Isolation with Migration model using a Markov chain Monte Carlo method. Rutgers university. http://lifesci.rutgers.edu/~heylab/programsandData/Programs/IM/IMdocumentation.pdf.
Hollocher, H. 1996. Island Hopping in Drosophila: Genetic Patterns and Speciation Mechanisms. 124-141 in P. R. Grant, ed. Evolution on Islands. Oxford University Press, New York.
Hudson, R. R., and N. L. Kaplan. 1985. Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111:147-164.
Hudson, R. R., M. Kreitman, and M. Aguade. 1987. A test of neutral molecular evolution based on nucleotide data. Genetics 116:153-159.
Jan, S., J. Wang, C.-S. Chern, and S.-Y. Cho. 2002. Seasonal variation of circulation in the Taiwan Strait. Journal of Marine Systems 35:249-268.
Kimura, M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16:111-120.
Klicka, J., and R. M. Zink. 1997. The importance of recent Ice Ages in speciation: a failed paradigm. Science 277:1666-1669.
Koh, H. S., W.-J. Lee, and T. D. Kocher. 2000. The genetic relationships of two subspecies of striped field mice, Apodemus agrarius coreae and Apodemus agrarius chejuensis. Heredity 85:30-36.
Kumar, S., K. Tamura, and M. Nei. 2004. MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Briefings in Bioinformatics 5:150-163.
Lambeck, K., and J. Chappell. 2001. Sea level change through the last glacial cycle. Science 292:679-686.
Lambeck, K., T. M. Esat, and E. K. Potter. 2002. Links between climate and sea levels for the past three million years. Nature 419:199-206.
Li, W.-H. 1997. Molecular Evolution. Sinauer Associates, Sunderland, MA.
Li, S.-H., J.-W. Li, L.-X. Han, C.-T. Yao, H. Shi, F.-M. Lei, and C.-W. Yen. Species delimitation in the Hwamei (Garrulax canorus). Ibis:in press.
Liang, W.-D., T. Y. Tang, Y. J. Yang, M. T. Ko, and W.-S. Chuang. 2003. Upper-ocean currents around Taiwan. Deep Sea Research Part II: Topical Studies in Oceanography 50:1085-1105.
Lin, S.-M., C. A. Chen, and K.-Y. Lue. 2002. Molecular phylogeny and biogeography of the grass lizards genus Takydromus (Reptilia: Lacertidae) of East Asia. Molecular Phylogenetics and Evolution 22:276-288.
MacKinnon, J., and K. Phillipps. 2000. A Field Guide to the Birds of China. Oxford University Press, Oxford, UK.
Maekawa, K., N. Lo, O. Kitade, T. Miura, and T. Matsumoto. 1999. Molecular phylogeny and geographic distribution of wood-feeding cockroaches in East Asian Islands. Molecular Phylogenetics and Evolution 13:360-376.
Mayr, E. 1963. Animal Species and Evolution. Belknap Press, Cambridge, MA.
Melnick, D. J., and G. A. Hoelzer. 1992. Differences in male and female macaque dispersal lead to contrasting distributions of nuclear and mitochondrial DNA variation. International Journal of Primatology 13:1-25.
Monsen, K. J., and M. S. Blouin. 2003. Genetic structure in a montane ranid frog: restricted gene flow and nuclear-mitochondrial discordance. Molecular Ecology 12:3275-3286.
Nei, M. 1987. Molecular Evolutionary Genetics. Columbia University Press, New York.
Nelson, J. B. 1978. The Sulidae / gannets and boobies. Oxford University Press, Oxford.
Nelson, J. B. 1966. The breeding biology of the Gannet Sula bassana on the Bass Rock, Scotland. Ibis 108:584-626.
Nielsen, R., and J. Wakeley. 2001. Distinguishing migration from isolation: a Markov chain Monte Carlo approach. Genetics 158:885-896.
Nolan, V., Jr. 1978. The ecology and behavior of the Prairie Warbler (Dendroica discolor). in O. Monographs, ed. American Ornithological Union, Washington, D.C.
Nyakaana, S., and P. Arctander. 1999. Population genetic structure of the African elephant in Uganda based on variation at mitochondrial and nuclear loci: evidence for male-biased gene flow. Molecular Ecology 8:1105-1115.
Price, T. D. and M. M. Bouvier. 2002. The evolution of F1 post-zygotic incompatibilities in birds. Evolution 56:2083-2089.
Raymond, M., and F. Rousset. 1995. Genepop (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity 86:248-249.
Rees, D. J., B. C. Emerson, P. Oromi, and G. M. Hewitt. 2001. The diversification of the genus Nesotes (Coleoptera: Tenebrionidae) in the Canary Islands: evidence from mtDNA. Molecular Phylogenetics and Evolution 21:321-326.
Robinson-Rechavi, M., and D. Huchon. 2000. RRTree: relative-rate tests between groups of sequences on a phylogenetic tree. Bioinformatics 16:296-297.
Rohling, E. J., M. Fenton, F. J. Jorissen, P. Bertrand, G. Ganssen, and J. P. Caulet. 1998. Magnitudes of sea-level lowstands of the past 500,000 years. Nature 394:162-165.
Rozas, J., J. C. Sanchez-DelBarrio, X. Messeguer, and R. Rozas. 2003. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496-2697.
Sandler, L., and E. Novitski. 1957. Meiotic drive as an evolutionary force. American Naturalist 91:105-110.
Sarich, V. M., and A. C. Wilson. 1973. Generation time and genomic evolution in primates. Science 179:1144-1147.
Sibley, C. G., and J. E. Ahlquist. 1990. Phylogeny and Classification of Birds. Yale University Press, New Haven, CT and London.
Sibuet, J. C., and S. K. Hsu. 1997. Geodynamics of the Taiwan arc-arc collision. Tectonophysics 274:221-251.
Sibuet, J. C., and S. K. Hsu. 2004. How was Taiwan created? Tectonophysics 379:159-181.
Slatkin, M. 1981. Fixation probabilities and fixation times in a subdivided population. Evolution 35:477-488.
Slatkin, M. 1982. Pleiotropy and parapatric speciation. Evolution 36:263-270.
Slatkin, M. 1987. Gene flow and the geographic structure of natural populations. Science 236:787-792.
Smith, T. B., R. K. Wayne, D. J. Girman, and M. W. Bruford. 1997. A role for ecotones in generating rainforest biodiversity. Science 276:1855-1857.
Sotka, E. E., J. P. Wares, J. A. Barth, R. K. Grosberg, and S. R. Palumbi. 2004. Strong genetic clines and geographical variation in gene flow in the rocky intertidal barnacle Balanus glandula. Molecular Ecology 13:2143-2156.
Stephens, M., and P. Scheet. 2005. Accounting for decay of linkage disequilibrium in haplotype inference and missing data imputation. American Journal of Human Genetics 76:449-462.
Stephens, M., N. J. Smith, and P. Donnelly. 2001. A new statistical method for haplotype reconstruction from population data. American Journal of Human Genetics 68:978-989.
Swofford, D. L. 2002. PAUP*: Phylogenetic Analysis Using Parsimony (and Other Methods) 4.0. Sinauer Associates, Sunderland, MA.
Tamura K., M. Nei. 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10:512–526.
Tu, H.-W., and L. L. Severinghaus. 2004. Geographic variation of the highly complex Hwamei (Garrulax canorus) songs. Zoological Studies 43:629-640.
Voris, H. K. 2000. Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. Journal of Biogeography 27:1153-1167.
Wakeley, J., and J. Hey. 1997. Estimating ancestral population parameters. Genetics 145:847-855.
Wall, J. D. 2003. Estimating ancestral population sizes and divergence times. Genetics 163:395-404.
Williams, M., D. Dunkerley, P. de Deckker, P. Kershaw, and J. Chappell. 1998. Quaternary Environment. Arnold Publishers, London.
Won, Y. J., and J. Hey. 2005. Divergence population genetics of chimpanzees. Molecular Biology and Evolution 22:297-307.
Woolfenden, G. E., and J. W. Fitzpatrick. 1984. The Florida Scrub Jay: Demography of a Cooperative-breeding Bird. Princeton University Press, Princeton, NJ.
Wright, S. 1922. Coefficients of inbreeding and relationship. American Naturalist 56:330-338
Wright, S. 1931. Evolution in Mendelian populations. Genetics 16:97-159.
Wu, C.- I. 2001. The genic view of the process of speciation. Journal of Evolutionary Biology 14:851-865.
Wu, C.-I and A. T. Beckenbach. 1983. Evidence for extensive genetic differentiation between the sex-ratio and the standard arrangement of Drosophila pseudoobscura and D. persimilis and identification of hybrid sterility factors. Genetics 105:71-86