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1 総説 Ecological speciation Kei W. Matsubayashi 1 and Naoyuki Fujiyama 2 1 The Faculty of Arts and Science, Kyushu University 2 Department of Biology, Faculty of Science, Yamagata University Abstract: Ecological speciation is a mode of speciation in which adaptation to different environments causes populations to diverge and develop reproductive isolation from each other. This classical hypothesis has matured in the field of evolutionary ecology with the accumulation of new empirical data. A full understanding of the mechanisms by which ecological speciation leads to biological diversification requires the synthesis of ideas from many different disciplines, including evolution, ecology, and genetics. In the present review, we introduce the definition of ecological speciation and discuss factors leading to population divergence, geographic conditions, differences among taxa, and isolating barriers unique to this type of speciation. We then compare ecological speciation with alternative non-ecological modes of speciation. Throughout the review, we identify the weak points of the current concept of ecological speciation, and propose future challenges in the study of the mechanisms of biological diversification. Keywords: divergent natural selection, gene flow, interspecific interaction, local adaptation, reproductive isolation matsubayashi.kei@artsci.kyushu-u.ac.jp 561

2 ecological speciation * 1 isolating barrier reproductive isolation Darwin Wallace Darwin and Wallace 1858 Mayr Dobzhansky 1937 Mayr 1942, 1947 Darwin that mystery of mysteries Darwin Schluter Ecology of Adaptive RadiationSchluter 2000a 2012 Nosil Ecological Speciation Nosil 2012 Ecological Speciation Nosil 2012 Harrison 2012 Coyne and Orr 2004 * 2 Mayr 1942, 1963 biological species concept BSC Futuyma 2013, p.509 Coyne and Orr 2004 Hausdorf 2011 *1 *2 562

3 1 a b c d e divergent natural selection Schluter, 2000a, 2001, 2009 Nosil, 2012 divergent selection divergent sexual selection stabilizing selection directional selection 1a-d disruptive selection = diversifying selection; Futuyma e Schluter 2000a, p.104 Maan and Seehausen 2011 Schluter

4 incipient species 1 2 3Nosil 2012, p.55 1 abiotic interspecific interaction biotic Doebeli and Dieckmann 2000 Barret et al frequencydependent Taper and Case 1992 Gurevitch et al Denno et al Doebeli 1996 Bolnick 2004 Bolnick and Lau 2008 Calsbeek and Smith 2008 Calsbeek 2009 Hendry et al Schluter 2000a reinforcement Dobzhansky 1937 Servedio and Noor 2003 Kirkpatrick 2001 Nosil 2012, p.66 mating signal 3 Boughman 2002 sensory drive Pundamilia spp. Terai et al Seehausen et al local adaptation Lenormand 2012 Kawecki and Ebert 2004 metapopulation Blanquart et al Lenormand 2012 allopatric parapatric sympatric arms race Smith and Benkman

5 Zovi et al Mimulus guttatus Lowry et al. 2008a Lowry and Willis 2010 Ainsliaea faurieana A. apiculata hybrid zone Watanabe et al Mitsui et al Heliconius Jiggins 2008 Mallet 2009 character displacement Schluter 2000a, 2000b ecological character displacement Pfennig and Pfennig 2005 Rice and Pfennig 2008 reproductive character displacement Noor 1995 Rundle et al Pfennig and Ryan 2006 Ortiz-Barrientos et al Schluter 2001 geographic variation Futuyma 2013, pp sympatric speciation Coyne and Orr 2004, p.126 McCoy 2003 allopatric speciation parapatric speciation Coyne and Orr 2004 Bush 1969 Barluenga et al Savolainen et al

6 松林 圭 藤山直之 図 2 複数の地理的条件における生態的種分化の進行状況と要因を模式的に示した 一般的に種分化は異所的なフェー ズで始まり 二次的接触を経て側所的あるいは同所的フェーズに移行すると仮定する 黒線は仮想集団間の時間経 過にともなう生殖隔離の強さの変化を例示している 中央の点線は集団が二次的に接触した時点を示し それより 左側は異所的なフェーズで起きる集団分化を 右側は側所的あるいは同所的フェーズで起きる集団分化を示す そ れぞれのフェーズで分化を促す分岐自然選択の要因と 分化に与える一般的な効果の相対的強度を灰色の枠内に示 す Rundle and Nosil 2005 を改変 種分化はそのプロセスのどこかで上記三つのうちの複数 分化に及ぼす地理的条件の影響を評価するという視点か の地理的条件を経験することが徐々に明らかになってき ら議論が進められてきた Rundle and Nosil 2005 生態 たことも この地理的な視点の限界を示した 例えば 的種分化の過程における地理的条件の変化とその際の分 Feder et al. 2003, 2005 Butlin et al さらに 多くの 化に関わる要因を図 2 に示した ここで一般的なモデル 近縁種間で様々な程度の遺伝子流動が存在することが明 となっている集団分化は 異所的な条件で始まり やが らかになったことも手伝って 定義の曖昧さに拍車がか てある程度分化した集団が二次的接触 secondary contact かり 地理的条件を主眼とした考え方は勢いを失ってい を経て 同所的あるいは側所的に生息するようになると った 理論研究においても 同所的種分化の実現可能性 いうものである Schluter 2001 Rundle and Nosil 2005 は特に 1990 年代から 2000 年代の初めにかけて大きな注 側所的および同所的種分化は この二次的接触の時点が 目を集めた話題であった 例えば Dieckmann and Doebeli 分化の最初期 図 2 では X 軸の値が左端 に位置する特 1999 Higashi et al Kondrashov and Kondrashov 殊な例となり 異所的種分化は二次的接触が種分化の完 1999 Dieckmann et al Gavrilets 2004 同所的種分 了時点まで起きない場合となる 異所的フェーズと同所 化理論についてのこれまでの知見を大ざっぱにまとめる 的フェーズにおける最大の相違は 集団間の遺伝子流動 と 特定の条件下では十分に可能だが それらの条件が の起こりやすさである 分岐自然選択はこの両方のフェ 自然条件下で揃う可能性はさほど高くないという 実証 ーズで分化を促進するが 二次的接触後はその要因とし データの少なさと一致する結論になっている なお 種 て 分化途上の近縁集団間での隔離の強化と相互作用が 分化の理論研究における最近の進展は Gavrilets 2014 加わる このように 二次的接触以降の種分化は 分岐 を参照されたい 選択による集団分化と遺伝子流動による集団融合の間の 生態的種分化においても 地理的条件は集団分化に大 綱引きを伴って進行することになる この遺伝子流動下 きな影響をおよぼす要因である しかし 生態的種分化は での形質の分岐 d ivergence with gene flow は それぞれの 異所 同所の両極端の地理的フェーズの間で可変的に分 集団に固有の選択によってのみ維持される または進行 化が進むことを前提としているため Schluter 2001 ど するため 分岐選択による種分化の強い証拠であるとさ の地理的条件で種分化が起きるかという視点ではなく れる Maynard Smith 1966 Räsänen and Hendry 2008 Via 566

7 2012 McCormack et al Timema cristinae ecotype Nosil et al habitat isolation premating isolation post-mating isolation sexual isolation Nosil 2007 Schluter * 3 immigrant inviability *3 Nosil et al a 3b Nosil et al ecological hybrid inviability* 4 3c extrinsic Rundle and Whitlock 2001 F 2 2 backcross 3d Hatfield and Schluter 1999 Rundle 2002 Egan and Funk 2009 Kuwajima et al Peccoud et al Henosepilachna diekei Matsubayashi et al. 2011, 2013 Fujiyama et al *4 ecological hybrid incompatibility, ecologically-dependent hybrid inviability, ecologically-dependent hybrid unfitness hybrid inviability ecological hybrid inviability 567

8 3 1 2 a b c F d B F N F 1 F 2 a Matsubayashi et al. 2011, 2013 Matsubayashi et al Matsubayashi et al temporal isolation pollinator isolation mechanical isolation Rundle and Nosil 2005 Matsubayashi et al ecological isolation Coyne and Orr 2004 magic trait Gavrilets 2004 Servedio et al Gasterosteus spp. 568

9 assortative mating Nagel and Schluter 1998 Boughman et al Satsuma Pareas iwasakii Hoso et al Servedio et al Ueshima and Asami 2003 Asami et al delayed inheritance Davison et al Orr 1991 Yamamichi and Sasaki 2013 Hoso et al Dieckmann and Doebeli 1999 Rundle and Nosil 2005 Matsubayashi et al intrinsic Boughman 2002 Kawata et al Servedio and Noor 2003 Hoskin et al lock and key Sota and Kubota 1998 Sota and Tanabe 2010 Masly intrinsic hybrid inviability intrinsic hybrid sterility intrinsic hybrid behavioral sterility chromosomal rearrangement Coyne and Orr 2004, p.256 Dobzhansky-Muller incompatibility DMI 4 DMI A B AABB 569

10 Matsubayashi and Katakura A a B b AaBb Bomblies and Weigel 2007 a b epistasis 4 A a B b AaBB aabb aabb aabb AAbb AaBb Bomblies and Weigel 2007 Presgraves 2007 DMI Schluter 2009 DMI Sambatti et al Funk et al Bolnick et al host shift Bush 1969 Berlocher and Feder 2002 Drès and Mallet 2002 Janz and Nylin 2008 Matsubayashi et al

11 Templeton 2008 Sobel et al * 5 mutation-order speciation Mani and Clarke 1990 Nosil and Flaxman 2011 DMI * 6 uniform selection Schluter 2009 sexual conflict Gavrilets 2000 Gavrilets and Hayashi 2005 Crespi and Nosil 2013 * *6 phenotypic plasticity Turesson 1922 Lowry 2012 variety Funk 2012 Lowry 571

12 2012 seasonal isolation Coyne and Orr pp Cozzolino and Widmer 2005 * 7 deceptive pollination Ophrys Xu et al Bateman et al Breitkopf et al Mitella M. furusei var. subramosa M. pauciflora Okuyama and Kato 2009 Okamoto et al * Langerhans and Riesch 2013 niche-conservatism Peterson et al Wiens 2004 Losos 2008 Sobel et al eco-geographic isolation Sobel et al Ramsey et al global information system GIS ecological niche modeling ENM Guisan and Thuiller 2005 Warren et al. 2008, 2010 Elith and Leathwick 2009 Kozak and Wiens 2006 McCormack et al Glennon et al

13 Giraud et al Hufford and Mazer 2003 Lowry et al. 2008b Ipomopsis >3100 m I. tenuituba <2900 m I. aggregata Campbell et al Campbell 2004 Inurois punctigera Yamamoto and Sota 2009 Yamamoto and Sota 2012 Tsuchida et al cytoplasmic incompatibility Bordenstain et al Coyne and Orr 2004, 573

14 p.279 social selection West- Eberhard 1983, 2014 Lyon and Montgomerie 2012 West-Eberhard 2014 Schluter 2009 Danchin and Wagner 2010 Orcinus orca Riesch et al de Bruyn et al Moura et al Boomsma and Nash 2014 Rabeling et al Gould 1989 Templeton 1980, 2008 parallel evolution parallel speciation Schluter and Nagel 1995 Darwin

15 Pfennig et al Thibert-Plante and Hendry 2011 Snell-Rood 2013 Forsman 2015 diffuse coevolution Grant and Grant 2011, p.164 adaptive radiation P. Nosil R. Riesch 2 JSPS 16H06178 Asami T, Cowie RH, Ohbayashi K (1998) Evolution of mirror images by sexually asymmetric mating behavior in hermaphroditic snails. The American Naturalist, 152: Barluenga M, Stölting KN, Salzburger W, Muschick M, Meyer A (2006) Sympatric speciation in Nicaraguan crater lake cichlid fish. Nature, 439: Barrett RDH, Rogers SM, Schluter D (2008) Natural selection on a major armor gene in threespine stickleback. Science, 322: Bateman RM, Hollingsworth PM, Preston J, Luo YB, Pridgeon AM, Chase MW (2003) Molecular phylogenetics and evolution of Orchidinae and selected Habenariinae (Orchidaceae). Botanical Journal of the Linnean Society, 142:1-40 Berlocher SH, Feder JL (2002) Sympatric speciation in phytophagous insects: moving beyond controversy? Annual review of entomology, 47: Blanquart F, Kaltz O, Nuismer SL, Gandon S (2013) A practical guide to measuring local adaptation. Ecology Letters, 16: Bolnick DI (2004) Can intraspecific competition drive disruptive selection? An experimental test in natural populations of sticklebacks. Evolution, 58: Bolnick DI, Near TJ, Wainwright PC (2006) Body size divergence promotes post-zygotic reproductive isolation in centrarchids. Evolutionary Ecology Research, 8: Bolnick DI, Lau OL (2008) Predictable patterns of disruptive selection in stickleback in postglacial lakes. The American Naturalist, 172:1-11 Bomblies K, Weigel D (2007) Hybrid necrosis: autoimmunity as a potential gene-flow barrier in plant species. Nature Reviews Genetics, 8: Boomsma JJ, Nash DR (2014) Evolution: sympatric speciation the eusocial way. Current Biology, 24:R798-R800 Bordenstein SR, O Hara FP, Werren JH (2001) Wolbachiainduced incompatibility precedes other hybrid incompatibilities in Nasonia. Nature, 409: Boughman JW (2002) How sensory drive can promote 575

16 speciation. Trends in Ecology & Evolution, 17: Boughman JW, Rundle HD, Schluter D (2005) Parallel evolution of sexual isolation in sticklebacks. Evolution, 59: Breitkopf H, Onstein RE, Cafasso D, Schlüter PM, Cozzolino S (2015) Multiple shifts to different pollinators fueled rapid diversification in sexually deceptive Ophrys orchids. New Phytologist, 207: Bush GL (1969) Sympatric host race formation and speciation in frugivorous flies of the genus Rhagoletis (Diptera, Tephritidae). Evolution, 23: Butlin RK, Galindo J, Grahame JW (2008) Sympatric, parapatric or allopatric: the most important way to classify speciation? Philosophical Transaction of the Royal Society B: Biological Sciences, 363: Calsbeek R (2009) Experimental evidence that competition and habitat use shape the individual fitness surface. Journal of Evolutionary Biology, 22: Calsbeek R, Smith TB (2008) Experimentally replicated disruptive selection on performance traits in a Caribbean lizard. Evolution, 62: Campbell DR (2004) Natural selection in Ipomopsis hybrid zones: implications for ecological speciation. New Phytologist, 161:83-90 Campbell DR, Waser NM, Meléndez-Ackerman EJ (1997) Analyzing pollinator-mediated selection in a plant hybrid zone: hummingbird visitation patterns on three spatial scales. The American Naturalist, 149: Coyne JA, Orr HA (2004) Speciation. Sunderland, MA: Sinauer Associates, USA Cozzolino S, Widmer A (2005) Orchid diversity: an evolutionary consequence of deception? Trends in Ecology & Evolution, 20: Crespi B, Nosil P (2013) Conflictual speciation: species formation via genomic conflict. Trends in Ecology & Evolution, 28:48-57 Danchin É, Wagner RH (2010) Inclusive heritability: combining genetic and non-genetic information to study animal behavior and culture. Oikos, 119: Darwin C (1859) The Origin of Species by Means of Natural Selection or the Preservation of Favoured Races in the Struggle for Life. John Murray, London Darwin C, Wallace A (1858) On the tendency of species to form varieties; and on the perpetuation of varieties and species by natural means of selection. Journal of the Proceedings of the Linnean Society of London. Zoology, 3:45-62 Davison A, Chiba S, Barton NH, Clarke B (2005) Speciation and gene flow between snails of opposite chirality. PLoS Biology, 3:e282 de Bruyn PJN, Tosh CA, Terauds A (2013) Killer whale ecotypes: is there a global model? Biological Reviews, 88:62-80 Denno RF, McClure, MS, Ott JR (1995) Interspecific interactions in phytophagous insects: competition reexamined and resurrected. Annual Review of Entomology, 40: Dieckmann U, Doebeli M (1999) On the origin of species by sympatric speciation. Nature, 400: Dieckmann U, Doebeli M, Metz JAJ, Tautz D (2004) Adaptive speciation. Cambridge University Press, UK Dobzhansky T (1937) Genetics and the Origin of Species. Columbia University Press, NY Doebeli M (1996) An explicit genetic model for ecological character displacement. Ecology, 77: Doebeli M, Dieckmann U (2000) Evolutionary branching and sympatric speciation caused by different types of ecological interactions. The American Naturalist, 156:S77-S101 Drès M, Mallet J (2002) Host races in plant-feeding insects and their importance in sympatric speciation. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 357: Egan SP, Funk DJ (2009) Ecologically dependent postmating isolation between sympatric host forms of Neochlamisus bebbianae leaf beetles. Proceedings of the National Academy of Sciences, 106: Elith J, Leathwick JR (2009) Species distribution models: ecological explanation and prediction across space and time. Annual Review of Ecology, Evolution, and Systematics, 40: Feder JL, Berlocher SH, Roethele JB, Dambroski H, Smith JJ, Perry WL, Gavrilovic V, Filchak KE, Rull J, Aluja M (2003) Allopatric genetic origins for sympatric host-plant shifts and race formation in Rhagoletis. Proceedings of the National Academy of Sciences, 100: Feder JL, Xie X, Rull J, Velez S, Forbes A, Leung B, Dambroski H, Filchak KE, Aluja M (2005) Mayr, Dobzhansky, and Bush and the complexities of sympatric speciation in Rhagoletis. Proceedings of the National Academy of Sciences, 102: Forsman A (2015) Rethinking phenotypic plasticity and its consequences for individuals, populations and species. Heredity. 115: Fujiyama N, Ueno H, Kahono S, Hartini S, Matsubayashi KW, Kobayashi N, Katakura H (2013) Distribution and differentiation of Henosepilachna diekei (Coleoptera: Coccinellidae) on two host-plant species across Java, Indonesia. Annals of the Entomological Society of America, 106: Funk DJ (2012) Of host forms and host races: terminological issues in ecological speciation. International Journal of Ecology, 2012: Funk DJ, Nosil P, Etges WJ (2006) Ecological divergence exhibits consistently positive associations with reproductive isolation across disparate taxa. Proceedings of the National Academy of Sciences of the United States of America, 103: Futuyma DJ (2013) Evolution, 3rd edition. Sinauer. Sunderland, USA 576

17 Gavrilets S (2000) Rapid evolution of reproductive barriers driven by sexual conflict. Nature, 403: Gavrilets S (2004) Fitness Landscapes and the Origin of Species. Princeton University Press Gavrilets S (2014) Models of speciation: where are we now? Journal of Heredity, 105: Gavrilets S, Hayashi TI (2005) Speciation and sexual conflict. Evolutionary Ecology, 19: Giraud T, Gladieux P, Gavrilets S (2010) Linking the emergence of fungal plant diseases with ecological speciation. Trends in Ecology & Evolution, 25: Glennon KL, Rissler LJ, Church SA (2012) Ecogeographic isolation: a reproductive barrier between species and between cytotypes in Houstonia (Rubiaceae). Evolutionary Ecology, 26: Gould SJ (1989) Wonderful life: the Burgess Shale and the nature of history. W. W. Norton & Co., New York Grant PR, Grant BR (2011) How and why species multiply: the radiation of Darwin s finches. Princeton University Press, USA Guisan A, Thuiller W (2005) Predicting species distribution: offering more than simple habitat models. Ecology Letters, 8: Gurevitch J, Morrow LL, Wallace A, Walsh JS (1992) A metaanalysis of competition in field experiments. The American Naturalist, 140: Harrison RG (2012) The language of speciation. Evolution, 66: Hatfield T, Schluter D (1999) Ecological speciation in sticklebacks: environment-dependent hybrid fitness. Evolution, 53: Hausdorf B (2011) Progress toward a general species concept. Evolution, 65: Hendry AP, Huber SK, De León LF, Herrel A, Podos J (2009) Disruptive selection in a bimodal population of Darwin's finches. Proceedings of the Royal Society of London B: Biological Sciences, 276: Higashi M, Takimoto G, Yamamura N (1999) Sympatric speciation by sexual selection. Nature, 402: Hoskin CJ, Higgie M, McDonald KR, Moritz C (2005) Reinforcement drives rapid allopatric speciation. Nature, 437: Hoso M, Asami T, Hori M (2007) Right-handed snakes: convergent evolution of asymmetry for functional specialization. Biology Letters, 3: Hoso M, Kameda Y, Wu SP, Asami T, Kato M, Hori M (2010) A speciation gene for left-right reversal in snails results in anti-predator adaptation. Nature Communications, 1:133 Hufford KM, Mazer SJ (2003) Plant ecotypes: genetic differentiation in the age of ecological restoration. Trends in Ecology & Evolution, 18: Janz N, Nylin S (2008) The oscillation hypothesis of host-plant range and speciation. In: Tilmon K (ed), Specialization, speciation, and radiation: the evolutionary biology of herbivorous insects, University of California Press, USA Jiggins CD (2008) Ecological speciation in mimetic butterflies. Bioscience, 58: Kawata M, Shoji A, Kawamura S, Seehausen O (2007) A genetically explicit model of speciation by sensory drive within a continuous population in aquatic environments. BMC Evolutionary Biology, 7:99 Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecology Letters, 7: Kirkpatrick M (2001) Reinforcement during ecological speciation. Proceedings of the Royal Society of London B: Biological Sciences, 268: Kondrashov AS, Kondrashov FA (1999) Interactions among quantitative traits in the course of sympatric speciation. Nature, 400: Kozak KH, Wiens JJ (2006) Does niche conservatism promote speciation? A case study in North American salamanders. Evolution, 60: Kuwajima M, Kobayashi N, Katoh T, Katakura H (2010) Detection of ecological hybrid inviability in a pair of sympatric phytophagous ladybird beetles (Henosepilachna spp.). Entomologia Experimentalis et Applicata, 134: Langerhans RB, Riesch R (2013) Speciation by selection: A framework for understanding ecology s role in speciation. Current Zoology, 59:31-52 Lenormand T (2012) From local adaptation to speciation: specialization and reinforcement. International Journal of Ecology, 2012: Losos JB (2008) Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecology Letters, 11: Lowry DB (2012) Ecotypes and the controversy over stages in the formation of new species. Biological Journal of the Linnean Society, 106: Lowry DB, Rockwood RC, Willis JH (2008a) Ecological reproductive isolation of coast and inland races of Mimulus guttatus. Evolution, 62: Lowry DB, Modliszewski JL, Wright KM, Wu CA, Willis JH (2008b) The strength and genetic basis of reproductive isolating barriers in flowering plants. Philosophical Transactions of the Royal Society B: Biological Sciences, 363: Lowry DB, Willis JH (2010) A widespread chromosomal inversion polymorphism contributes to a major life-history transition, local adaptation, and reproductive isolation. PLoS Biology, 8:e Lyon BE, Montgomerie R (2012) Sexual selection is a form of social selection. Philosophical Transactions of the Royal Society B: Biological Sciences, 367: Maan ME, Seehausen O (2011) Ecology, sexual selection and speciation. Ecology Letters, 14: Mallet J (2009) Rapid speciation, hybridization and adaptive 577

18 radiation in the Heliconius melpomene group. In: Butlin R, Bridle J, Schluter D (ed), Speciation and patterns of diversity, Cambridge University Press, UK Mani GS, Clarke BC (1990) Mutational order: a major stochastic process in evolution. Proceedings of the Royal Society of London. B. Biological Sciences, 240:29-37 Masly JP (2011) 170 Years of Lock-and-Key : Genital morphology and reproductive isolation. International Journal of Evolutionary Biology, 2012, Matsubayashi KW, Katakura H (2009) Contribution of multiple isolating barriers to reproductive isolation between a pair of phytophagous ladybird beetles. Evolution, 63: Matsubayashi KW, Ohshima I, Nosil P (2010) Ecological speciation in phytophagous insects. Entomologia Experimentalis et Applicata, 134:1-27 Matsubayashi KW, Kahono S, Katakura H (2011) Divergent host plant specialization as the critical driving force in speciation between populations of a phytophagous ladybird beetle. Journal of Evolutionary Biology, 24: Matsubayashi KW, Kahono S, Katakura H (2013) Divergent host plant preference causes assortative mating between sympatric host races of the ladybird beetle, Henosepilachna diekei. Biological Journal of the Linnean Society, 110: Maynard Smith J (1966) Sympatric speciation. The American Naturalist, 100: Mayr E (1942) Systematics and the origin of species, from the viewpoint of a zoologist. Harvard University Press, London Mayr E (1947) Ecological factors in speciation. Evolution, 1: Mayr E (1963) Animal species and evolution. Harvard University Press, London McCormack JE, Zellmer AJ, Knowles LL (2010) Does niche divergence accompany allopatric divergence in Aphelocoma jays as predicted under ecological speciation?: insights from tests with niche models. Evolution, 64: McCoy KD (2003) Sympatric speciation in parasites-what is sympatry? Trends in Parasitology, 19: Mitsui Y, Nomura N, Isagi Y, Tobe H, Setoguchi H (2011) Ecological barriers to gene flow between riparian and forest species of Ainsliaea (Asteraceae). Evolution, 65: ,, (2012)., Moura AE, Kenny JG, Chaudhuri R, Hughes MA, Welch AJ, Reisinger RR, de Bruyn PJN, Dahlheim ME, Hall N, Rus Hoelzel A (2014) Population genomics of the killer whale indicates ecotype evolution in sympatry involving both selection and drift. Molecular Ecology, 23: Nagel L, Schluter D (1998) Body size, natural selection, and speciation in sticklebacks. Evolution, 52: Noor MA (1995) Speciation driven by natural selection in Drosophila. Nature, 375: Nosil P (2007) Divergent host plant adaptation and reproductive isolation between ecotypes of Timema cristinae walking sticks. The American Naturalist, 169: Nosil P (2012) Ecological speciation. Oxford University Press, New York Nosil P, Crespi BJ, Sandoval CP (2002) Host-plant adaptation drives the parallel evolution of reproductive isolation. Nature, 417: Nosil P, Vines TH, Funk DJ (2005) Reproductive isolation caused by natural selection against immigrants from divergent habitats. Evolution, 59: Nosil P, Flaxman SM (2011) Conditions for mutation-order speciation. Proceedings of the Royal Society B: Biological Sciences, 278: Okamoto T, Okuyama Y, Goto R, Tokoro M, Kato M (2015) Parallel chemical switches underlying pollinator isolation in Asian Mitella. Journal of Evolutionary Biology, 28: Okuyama Y, Kato M (2009) Unveiling cryptic species diversity of flowering plants: successful biological species identification of Asian Mitella using nuclear ribosomal DNA sequences. BMC Evolutionary Biology, 9:105 Orr HA (1991) Is single-gene speciation possible? Evolution, 45: Ortiz-Barrientos D, Grealy A, Nosil P (2009) The genetics and ecology of reinforcement. Annals of the New York Academy of Sciences, 1168: Peccoud J, de la Huerta M, Bonhomme J, Laurence C, Outreman Y, Smadja CM, Simon JC (2014) Widespread host-dependent hybrid unfitness in the pea aphid species complex. Evolution, 68: Peterson AT, Soberón J, Sánchez-Cordero V (1999) Conservatism of ecological niches in evolutionary time. Science, 285: Pfennig KS, Pfennig DW (2005) Character displacement as the best of a bad situation : fitness trade-offs resulting from selection to minimize resource and mate competition. Evolution, 59: Pfennig KS, Ryan MJ (2006) Reproductive character displacement generates reproductive isolation among conspecific populations: an artificial neural network study. Proceedings of the Royal Society of London B: Biological Sciences, 273: Pfennig DW, Wund MA, Snell-Rood EC, Cruickshank T, Schlichting CD, Moczek AP (2010) Phenotypic plasticity s impacts on diversification and speciation. Trends in Ecology & Evolution, 25: Presgraves DC (2007) Speciation genetics: epistasis, conflict and the origin of species. Current Biology, 17:R125-R127 Rabeling C, Schultz TR, Pierce NE, Bacci M Jr (2014) A social parasite evolved reproductive isolation from its fungusgrowing ant host in sympatry. Current Biology, 24: Ramsey J, Bradshaw HD, Schemske DW (2003) Components of reproductive isolation between the monkeyflowers Mimulus lewisii and M. cardinalis (Phrymaceae). Evolution, 57:

19 Räsänen K, Hendry AP (2008) Disentangling interactions between adaptive divergence and gene flow when ecology drives diversification. Ecology Letters, 11: Rice AM, Pfennig DW (2008) Analysis of range expansion in two species undergoing character displacement: why might invaders generally win during character displacement? Journal of Evolutionary Biology, 21: Riesch R, Barrett-Lennard LG, Ellis GM, Ford JKB, Deecke VB (2012) Cultural traditions and the evolution of reproductive isolation: ecological speciation in killer whales? Biological Journal of the Linnean Society, 106:1-17 Rundle HD (2002) A test of ecologically dependent postmating isolation between sympatric sticklebacks. Evolution, 56: Rundle HD, Whitlock MC (2001) A genetic interpretation of ecologically dependent isolation. Evolution, 55: Rundle HD, Vamosi SM, Schluter D (2003) Experimental test of predation's effect on divergent selection during character displacement in sticklebacks. Proceedings of the National Academy of Sciences, 100: Rundle HD, Nosil P (2005) Ecological speciation. Ecology Letters, 8: Sambatti JBM, Ortiz-Barrientos D, Baack EJ, Rieseberg LH (2008) Ecological selection maintains cytonuclear incompatibilities in hybridizing sunflowers. Ecology Letters, 11: Savolainen V, Anstett MC, Lexer C, Hutton I, Clarkson JJ, Norup MV, Powell MP, Springate D, Salamin N, Baker WJ (2006) Sympatric speciation in palms on an oceanic island. Nature, 441: Schluter D (2000a) The ecology of adaptive radiation. Oxford University Press, New York Schluter D (2000b) Ecological character displacement in adaptive radiation. The American Naturalist, 156:S4-S16 Schluter D (2001) Ecology and the origin of species. Trends in Ecology & Evolution, 16: Schluter D (2009) Evidence for ecological speciation and its alternative. Science, 323: Schluter D, Nagel LM (1995) Parallel speciation by natural selection. The American Naturalist, 146: Seehausen O, Terai Y, Magalhaes IS, Carleton KL, Mrosso HDJ, Miyagi R, van der Sluijs I, Schneider MV, Maan ME, Tachida H, Imai H, Okada N (2008) Speciation through sensory drive in cichlid fish. Nature, 455: Servedio MR, Noor MAF (2003) The role of reinforcement in speciation: theory and data. Annual Review of Ecology, Evolution, and Systematics, 34: Servedio MR, Van Doorn GS, Kopp M, Frame AM, Nosil P (2011) Magic traits in speciation: magic but not rare? Trends in Ecology & Evolution, 26: Smith JW, Benkman CW (2007) A coevolutionary arms race causes ecological speciation in crossbills. The American Naturalist, 169: Snell-Rood EC (2013) An overview of the evolutionary causes and consequences of behavioural plasticity. Animal Behaviour, 85: Sobel JM, Chen GF, Watt LR, Schemske DW (2010) The biology of speciation. Evolution, 64: Sota T, Kubota K (1998) Genital lock-and-key as a selective agent against hybridization. Evolution, 52: Sota T, Tanabe T (2010) Multiple speciation events in an arthropod with divergent evolution in sexual morphology. Proceedings of the Royal Society B: Biological Sciences, 277: (2002). (,, ), , Taper ML, Case TJ (1992) Models of character displacement and the theoretical robustness of taxon cycles. Evolution, 46: Templeton AR (1980) The theory of speciation via the founder principle. Genetics, 94: Templeton AR (2008) The reality and importance of founder speciation in evolution. Bioessays, 30: Terai Y, Seehausen O, Sasaki T, Takahashi K, Mizoiri S, Sugawara T, Sato T, Watanabe M, Konijnendijk N, Mrosso HDJ, Tachida H, Imai H, Shichida Y, Okada N (2006) Divergent selection on opsins drives incipient speciation in Lake Victoria cichlids. PLoS Biology, 4:e433 Thibert-Plante X, Hendry AP (2011) The consequences of phenotypic plasticity for ecological speciation. Journal of Evolutionary Biology, 24: Tsuchida T, Koga R, Fukatsu T (2004) Host plant specialization governed by facultative symbiont. Science, 303:1989 Turesson, G (1922) The species and the variety as ecological units. Hereditas, 3: Ueshima R, Asami T (2003) Single-gene speciation by leftright reversal. Nature, 425:679 Via S (2012) Divergence hitchhiking and the spread of genomic isolation during ecological speciation-with-geneflow. Philosophical Transactions of the Royal Society B: Biological Sciences, 367: Warren DL, Glor RE, Turelli M (2008) Environmental niche equivalency versus conservatism: quantitative approaches to niche evolution. Evolution, 62: Warren DL, Glor RE, Turelli M (2010) ENMTools: a toolbox for comparative studies of environmental niche models. Ecography, 33: Watanabe K, Yahara T, Kadota H (1992) Natural hybrid populations between chasmogamous and cleistogamous species, Ainsliaea faurieana and A. apiculata (Asteraceae; Mutisiae): morphology, cytology, reproductive mode and allozyme variation. Plant Species Biology, 7:49-59 West-Eberhard MJ (1983) Sexual selection, social competition, and speciation. Quarterly Review of Biology, 58: West-Eberhard MJ (2014) Darwin s forgotten idea: The social essence of sexual selection. Neuroscience & Biobehavioral Reviews, 46:

20 Wiens JJ (2004) Speciation and ecology revisited: phylogenetic niche conservatism and the origin of species. Evolution, 58: Xu S, Schlüter PM, Schiestl FP (2012) Pollinator-driven speciation in sexually deceptive orchids. International Journal of Ecology, 2012: Yamamichi M, Sasaki A (2013) Single-gene speciation with pleiotropy: effects of allele dominance, population size, and delayed inheritance. Evolution, 67: Yamamoto S, Sota T (2009) Incipient allochronic speciation by climatic disruption of the reproductive period. Proceedings of the Royal Society B: Biological Sciences, 276: Yamamoto S, Sota T (2012) Parallel allochronic divergence in a winter moth due to disruption of reproductive period by winter harshness. Molecular Ecology, 21: Zovi D, Stastny M, Battisti A, Larsson S (2008) Ecological costs on local adaptation of an insect herbivore imposed by host plants and enemies. Ecology, 89: