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On the Evolutionary Developmental Biology of Speciation

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Abstract

The mainstream approaches to the study of speciation and clade diversification have extensively focused on genetic mechanisms and ecological contexts, while much less attention has been paid to the role of development. In this paper we provide materials to support the thesis that taking development into the picture of evolutionary processes can bring important insights on how species multiply and diversify. Evidence that developmentally entangled evolutionary factors are important in speciation comes from different lines of investigation that can be broadly grouped under three headings: evolvability, phenotypic plasticity, and phenology. Evolvability enters the scene through the complexity of the genotype-phenotype map, the developmental link between transmissible genetic information and selectable phenotypes. Phenotypic plasticity can act as a facilitator for speciation, promoting diversification at different stages of the speciation process, as well as generating novel targets and novel trade-offs for evolutionary processes. The formal inclusion of the developmental time axis in speciation models widens the scope for investigating the onset and/or reinforcement of reproductive barriers through a range of situations along an organism’s life cycle. Overall, developmental processes can contribute to speciation and diversification at different stages of the speciation process, at different levels of biological organization and along the organism’s whole life cycle.

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References

  • Abzhanov, A., Kuo, W. P., Hartmann, C., Grant, B. R., Grant, P. R., & Tabin, C. J. (2006). The calmodulin pathway and evolution of elongated beak morphology in Darwin’s finches. Nature, 442, 563–567.

    Article  PubMed  CAS  Google Scholar 

  • Abzhanov, A., Protas, M., Grant, B. R., Grant, P. R., & Tabin, C. J. (2004). Bmp4 and morphological variation of beaks in Darwin’s finches. Science, 305, 1462–1465.

    Article  PubMed  CAS  Google Scholar 

  • Adams, K. L., & Wendel, J. F. (2005). Polyploidy and genome evolution in plants. Current Opinions in Plant Biology, 8, 135–141.

    Article  CAS  Google Scholar 

  • Alberch, P. (1991). From genes to phenotype: Dynamical systems and evolvability. Genetica, 84, 5–11.

    Article  PubMed  CAS  Google Scholar 

  • Alexander, R. D. (1968). Life cycle origins, speciation, and related phenomena in crickets. Quarterly Review of Biology, 43, 1–41.

    Article  PubMed  CAS  Google Scholar 

  • Alexander, R. D., & Bigelow, R. S. (1960). Allochronic speciation in field crickets, and a new species, Acheta veletis. Evolution, 14, 334–346.

    Article  Google Scholar 

  • Bell, M. A. (1974). Reduction and loss of the pelvic girdle in Gasterosteus (Pisces): A case of parallel evolution. Los Angeles: Natural History Museum, Los Angeles County.

    Google Scholar 

  • Bernatchez, L., Vuorinen, J. A., Bodaly, R. A., & Dodson, J. J. (1996). Genetic evidence for reproductive isolation and multiple origins of sympatric trophic ecotypes of whitefish (Coregonus). Evolution, 50, 624–635.

    Article  Google Scholar 

  • Bonato, L., Foddai, D., & Minelli, A. (2001). Increase by duplication and loss of invariance of segment number in the centipede Mecistocephalus microporus Haase, 1887 (Chilopoda, Geophilomorpha, Mecistocephalidae). Italian Journal of Zoology, 68, 345–352.

    Article  Google Scholar 

  • Bonato, L., Foddai, D., & Minelli, A. (2003). Evolutionary trends and patterns in centipede segment number based on a cladistic analysis of Mecistocephalidae (Chilopoda: Geophilomorpha). Systematic Entomology, 28, 539–579.

    Article  Google Scholar 

  • Box, M. S., Bateman, R. M., Glover, B. J., & Rudall, P. J. (2008). Floral ontogenetic evidence of repeated speciation via paedomorphosis in subtribe Orchidinae (Orchidaceae). Botanical Journal of the Linnean Society, 157, 429–454.

    Article  Google Scholar 

  • Briggs, D., & Walters, S. M. (1997). Plant variation and evolution (3rd ed.). Cambridge: Cambridge University Press.

    Google Scholar 

  • Butlin, R. K., Galindo, J., & Grahame, J. W. (2008). Sympatric, parapatric or allopatric: The most important way to classify speciation? Philosophical Transactions of the Royal Society Series B, 363, 2997–3007.

    Article  Google Scholar 

  • Carlquist, S. (1974). Island biology. New York, NY: Columbia University Press.

    Google Scholar 

  • Carlquist, S. (1980). Hawaii. A natural history (2nd ed.). Kauai, Hawaii: Pacific Tropical Botanical Garden.

    Google Scholar 

  • Chagas, A., Jr, Edgecombe, G. D., & Minelli, A. (2008). Variability in trunk segmentation in the centipede order Scolopendromorpha: A remarkable new species of Scolopendropsis Brandt (Chilopoda: Scolopendridae) from Brazil. Zootaxa, 1888, 36–46.

    Google Scholar 

  • Colosimo, P. F., Hosemann, K. E., Balabhadra, S., Villarreal, G., Jr, Dickson, M., Grimwood, J., et al. (2005). Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles. Science, 307, 1928–1933.

    Article  PubMed  CAS  Google Scholar 

  • Cook, S. A., & Johnson, M. P. (1968). Adaptation to heterogeneous environments. I. Variation in heterophylly in Ranunculus flammea L. Evolution, 22, 496–516.

    Article  Google Scholar 

  • Coyne, J. A., & Orr, H. A. (2004). Speciation. Sunderland, MA: Sinauer Associates.

    Google Scholar 

  • Crow, K. D., Stadler, P. F., Lynch, V. J., Amemiya, C., & Wagner, G. P. (2006). The “fish-specific” Hox cluster duplication is coincident with the origin of teleosts. Molecular Biology and Evolution, 23, 121–136.

    Article  PubMed  CAS  Google Scholar 

  • Davison, A., Chiba, S., Barton, N. H., & Clarke, B. (2005). Speciation and gene flow between snails of opposite chirality. PLoS Biology, 3(9), e282.

    Article  PubMed  CAS  Google Scholar 

  • De Bodt, S., Maere, S., & Van de Peer, Y. (2005). Genome duplication and the origin of angiosperms. Trends in Ecology and Evolution, 20, 591–597.

    Article  PubMed  Google Scholar 

  • de Soó, R. & Webb, D. A. (1972). Melampyrum L.; Rhinanthus L. In T. G. Tutin, V. H. Heywood, N. A. Burges, D. M Moore, D. H. Valentine, S. M. Walters, & D. A Webb (Eds.), Flora Europaea (Vol. 3, pp. 252–257; 276–280). Cambridge: Cambridge University Press.

  • Denoël, M., Joly, P., & Whiteman, H. H. (2005). Evolutionary ecology of facultative paedomorphosis in newts and salamanders. Biological Reviews, 80, 663–671.

    Article  PubMed  Google Scholar 

  • Denoël, M., Poncin, P., & Ruwet, J. C. (2001). Sexual compatibility between two heterochronic morphs in the Alpine newt, Triturus alpestris. Animal Behaviour, 62, 559–566.

    Article  Google Scholar 

  • Douglas, M. R., Brunner, P. C., & Douglas, M. E. (2005). Evolutionary homoplasy among species flocks of central Alpine Coregonus (Teleostei: Salmoniformes). Copeia, 2005, 347–358.

    Article  Google Scholar 

  • Eberhard, W. G. (1985). Sexual selection and animal genitalia. Cambridge, MA: Harvard University Press.

    Google Scholar 

  • Eberhard, W. G., Huber, B. A., Rodriguez, R. L., Briceno, R. D., & Rodriguez, V. (1998). One size fits all? Relationships between the size and degree of variation in genitalia and other body parts in twenty species of insects and spiders. Evolution, 52, 415–431.

    Article  Google Scholar 

  • Felsenstein, J. (1981). Skepticism toward Santa Rosalia, or why are there so few kinds of animals? Evolution, 35, 124–138.

    Article  Google Scholar 

  • Fitzpatrick, B. M., Fordyce, J. A., & Gavrilets, S. (2008). What, if anything, is sympatric speciation? Journal of Evolutionary Biology, 21, 1452–1459.

    Article  PubMed  CAS  Google Scholar 

  • Fusco, G. (2001). How many processes are responsible for phenotypic evolution? Evolution & Development, 3, 279–286.

    Article  CAS  Google Scholar 

  • Fusco, G., & Minelli, A. (2010). Phenotypic plasticity in development and evolution: facts and concepts. Philosophical Transactions of the Royal Society Series B, 365, 547–556.

    Article  Google Scholar 

  • Gittenberger, E. (1988). Sympatric speciation in snails. A largely neglected model. Evolution, 42, 826–828.

    Article  Google Scholar 

  • Grant, P. R. (1999). The ecology and evolution of Darwin’s finches. Princeton, NJ: Princeton University Press.

    Google Scholar 

  • Grant, P. R., & Grant, B. R. (2002). Unpredictable evolution in a 30-year study of Darwin’s finches. Science, 296, 707–711.

    Article  PubMed  CAS  Google Scholar 

  • Grant, P. R., & Grant, B. R. (2008). How and why species multiply: The radiation of Darwin’s finches. Princeton, NJ: Princeton University Press.

    Google Scholar 

  • Hawthorne, D. J., & Via, S. (2001). Genetic linkage of ecological specialization and reproductive isolation in pea aphids. Nature, 412, 904–907.

    Article  PubMed  CAS  Google Scholar 

  • Heard, S. B., & Hauser, D. L. (1995). Key evolutionary innovations and their ecological mechanisms. Historical Biology, 10, 151–173.

    Article  Google Scholar 

  • Heliövaara, K., & Väisänen, R. (1987). Geographic variation in the life-history of Aradus cinnamomeus and a breakdown of the reproductive isolation of allochronic bugs (Heteroptera, Aradidae). Annales Zoologici Fennici, 24, 1–17.

    Google Scholar 

  • Heliövaara, K., Väisänen, R., Hantula, J., Lokki, J., & Saura, A. (1988). Genetic differentiation in sympatric but temporally isolated pine bark bugs, Aradus cinnamomeus (Heteroptera). Hereditas, 109, 29–36.

    Article  Google Scholar 

  • Heliövaara, K., Väisänen, R., & Simon, C. (1994). Evolutionary ecology of periodical insects. Trends in Ecology and Evolution, 9, 475–480.

    Article  PubMed  Google Scholar 

  • Hendrikse, J. L., Parsons, T. E., & Hallgrímsson, B. (2007). Evolvability as the proper focus of evolutionary developmental biology. Evolution & Development, 9, 393–401.

    Article  Google Scholar 

  • Hoekstra, H. E., & Coyne, J. A. (2007). The locus of evolution: Evo devo and the genetics of adaptation. Evolution, 61, 955–1016.

    Article  Google Scholar 

  • Holland, L. Z., Albalat, R., Azumi, K., Benito-Gutiérrez, E., Blow, M. J., Bronner-Fraser, M., et al. (2008). The amphioxus genome illuminates vertebrate origins and cephalochordate biology. Genome Research, 18, 1100–1111.

    Article  PubMed  CAS  Google Scholar 

  • Jablonski, D. (2005). Evolutionary innovations in the fossil record: the intersection of ecology, development and macroevolution. Journal of Experimental Zoology B, Molecular and Developmental Evolution, 304B, 504–519.

    Article  Google Scholar 

  • Johnson, M. S., Clarke, B., & Murray, J. (1990). The coil polymorphism in Partula suturalis does not favor sympatric speciation. Evolution, 44, 459–464.

    Article  Google Scholar 

  • Keller, E. F. (2000). The century of the gene. Cambridge: Harvard University Press.

    Google Scholar 

  • Kellis, M., Birren, B. W., & Lander, E. S. (2004). Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature, 428, 617–624.

    Article  PubMed  CAS  Google Scholar 

  • Kliman, R. M., Andolfatto, P., Coyne, J. A., Depaulis, F., Kreitman, M., Berry, A. J., et al. (2000). The population genetics of the origin and divergence of the Drosophila simulans complex species. Genetics, 156, 1913–1931.

    PubMed  CAS  Google Scholar 

  • Kopp, A. (2011). Drosophila sex combs as a model of evolutionary innovation. Evolution & Development, 13, 504–522.

    Article  Google Scholar 

  • Krenz, J. D., & Verrell, P. A. (2002). Integrity in the midst of sympatry: does sexual incompatibility facilitate the coexistence of metamorphic and paedomorphic mole salamanders (Ambystoma talpoideum)? Journal of Zoology, 258, 435–440.

    Article  Google Scholar 

  • Kupiec, J.-J. (2009). The origins of individuals. Singapore: World Scientific.

    Book  Google Scholar 

  • Landry, L., Vincent, W. F., & Bernatchez, L. (2007). Parallelism between limnological features and phenotypic evolution of lake whitefish dwarf ecotypes. Journal of Evolutionary Biology, 20, 971–984.

    Article  PubMed  CAS  Google Scholar 

  • Lennartsson, T. (1997). Seasonal differentiation—a conservative reproductive barrier in two grassland Gentianella (Gentianaceae) species. Plant Systematics and Evolution, 208, 45–69.

    Article  Google Scholar 

  • Lu, G., & Bernatchez, L. (1999). Correlated trophic specialization and genetic divergence in sympatric lake whitefish ecotypes (Coregonus clupeaformis): Support for the ecological speciation hypothesis. Evolution, 53, 1491–1505.

    Article  Google Scholar 

  • Mallet, J. (2008). Hybridization, ecological races and the nature of species: Empirical evidence for the ease of speciation. Philosophical Transactions of the Royal Society Series B, 363, 2971–2986.

    Article  Google Scholar 

  • Mallet, J., Meyer, A., Nosil, P., & Feder, J. L. (2009). Space, sympatry and speciation. Journal of Evolutionary Biology, 22, 2332–2341.

    Article  PubMed  CAS  Google Scholar 

  • Marshall, D. C., & Cooley, J. R. (2000). Reproductive character displacement and speciation of a new species, 13-year Magicicada neotredecim. Evolution, 54, 1313–1325.

    PubMed  CAS  Google Scholar 

  • Marshall, D. C., Cooley, J. R., & Hill, K. B. R. (2011). Developmental plasticity of life-cycle length in thirteen-year periodical cicadas (Hemiptera: Cicadidae). Annals of the Entomological Society of America, 104, 443–450.

    Article  Google Scholar 

  • Martin, A. P., & Simon, C. (1988). Anomalous distribution of nuclear and mitochondrial DNA markers in periodical cicadas. Nature, 336, 237–239.

    Article  Google Scholar 

  • Martin, A., & Simon, C. (1990a). Differing levels of among population divergence in the mitochondrial DNA of periodical cicadas related to historical biogeography. Evolution, 44, 1066–1080.

    Article  Google Scholar 

  • Martin, A., & Simon, C. (1990b). Temporal variation in insect life cycles. BioScience, 40, 359–367.

    Article  Google Scholar 

  • Maynard Smith, J. (1970). Sympatric speciation. American Naturalist, 104, 487–490.

    Article  Google Scholar 

  • Mayr, E. (1960). The emergence of evolutionary novelties. In S. Tax (Ed.), Evolution after Darwin (pp. 349–380). Chicago, IL: University of Chicago Press.

    Google Scholar 

  • Meusel, H., & Kästner, A. (1990). Lebensgeschichte der Gold- und Silberdisteln. Monographie der mediterran-mitteleuropäischen Compositen-Gattung Carlina. Wien-New York: Springer.

    Book  Google Scholar 

  • Mikó, I., Friedrich, F., Yoder, M. J., Hines, H. M., Deitz, L. L., Bertone, M. A., et al. (2012). On dorsal prothoracic appendages in treehoppers (Hemiptera: Membracidae) and the nature of morphological evidence. PLoS One, 7(1), e30137.

    Article  PubMed  CAS  Google Scholar 

  • Minelli, A., Chagas-Júnior, A., & Edgecombe, G. D. (2009). Saltational evolution of trunk segment number in centipedes. Evolution & Development, 11, 318–322.

    Article  Google Scholar 

  • Minelli, A., & Fusco, G. (2005). Conserved versus innovative features in animal body organization. Journal of Experimental Zoology B, Molecular and Developmental Evolution, 304B, 520–525.

    Article  Google Scholar 

  • Minelli, A., & Fusco, G. (eds) (2008). Evolving pathways. Key themes in evolutionary developmental biology. Cambridge University Press, Cambridge.

  • Moczek, A. P. (2008). On the origins of novelty in development and evolution. BioEssays, 30, 432–447.

    Article  PubMed  Google Scholar 

  • Moczek, A. P. (2009). On the origins of novelty and diversity in development and evolution: A case study on beetle horns. Cold Spring Harbor Symposia on Quantitative Biology, 74, 289–296.

    Article  PubMed  CAS  Google Scholar 

  • Moczek, A. P. (2010). Phenotypic plasticity and diversity in insects. Philosophical Transactions of the Royal Society Series B, 365, 593–603.

    Article  Google Scholar 

  • Moczek, A. P., & Rose, D. J. (2009). Differential recruitment of limb patterning genes during development and diversification of beetle horns. Proceedings of the National Academy of Sciences of the United States of America, 106, 8992–8997.

    Article  PubMed  CAS  Google Scholar 

  • Moczek, A. P., Sultan, S., Foster, S., Ledón-Rettig, C., Dworkin, I., Nijhout, H. F., et al. (2011). The role of developmental plasticity in evolutionary innovation. Proceedings of the Royal Society B Biological Sciences, 278, 2705–2713.

    Article  Google Scholar 

  • Müller, G. B. (1990). Developmental mechanisms at the origin of morphological novelty: a side-effect hypothesis. In M. H. Nitecki (Ed.), Evolutionary innovations (pp. 99–130). Chicago, IL: University of Chicago Press.

    Google Scholar 

  • Müller, G. B., & Wagner, G. P. (1991). Novelty in evolution: Restructuring the concept. Annual Review of Ecology and Systematics, 22, 229–256.

    Article  Google Scholar 

  • Müller, G. B., & Wagner, G. P. (2003). Innovation. In B. K. Hall & W. M. Olson (Eds.), Keywords and concepts in evolutionary developmental biology (pp. 218–227). Cambridge, MA: Harvard University Press.

    Google Scholar 

  • Murphy, H. A., & Zeyl, C. W. (2012). Prezygotic isolation between Saccharomyces cerevisiae and Saccharomyces paradoxus through differences in mating speed and germination timing. Evolution, 66, 1196–1209.

    Article  PubMed  Google Scholar 

  • Naisbit, R. E., Jiggins, C. D., & Mallet, J. (2003). Mimicry: developmental genes that contribute to speciation. Evolution & Development, 5, 269–280.

    Article  CAS  Google Scholar 

  • Nielsen, M. G., Wilson, K. A., Raff, E. C., & Raff, R. A. (2000). Novel gene expression patterns in hybrid embryos between species with different modes of development. Evolution & Development, 2, 133–144.

    Article  CAS  Google Scholar 

  • Nijhout, H. F., & Emlen, D. J. (1998) Competition among body parts in the development and evolution of insect morphology. Proceedings of the National Academy of Sciences of the United states of America, 95, 3685–3689.

    Article  Google Scholar 

  • Nolte, A. W., Renaut, S., & Bernatchez, L. (2009). Divergence in gene regulation at young life history stages of whitefish (Coregonus sp.) and the emergence of genomic isolation. BMC Evolutionary Biology, 9, 59.

    Article  PubMed  CAS  Google Scholar 

  • Østbye, K., Amundsen, P.-A., Bernatchez, L., Klemetsen, A., Knudsen, R., Kristoffersen, R., et al. (2006). Parallel evolution of ecomorphological traits in the European whitefish Coregonus lavaretus (L.) species complex during postglacial times. Molecular Ecology, 15, 3983–4001.

    Article  PubMed  CAS  Google Scholar 

  • Østbye, K., Næsje, T. F., Bernatchez, L., Sandlund, O. T., & Hindar, K. (2005). Morphological divergence and origin of sympatric populations of European whitefish (Coregonus lavaretus L.) in Lake Femund, Norway. Journal of Evolutionary Biology, 18, 683–702.

    Article  PubMed  Google Scholar 

  • Parks, A. L., Parr, B. A., Chin, J.-E., Leaf, D. S., & Raff, R. A. (1988). Molecular analysis of heterochronic changes in the evolution of direct developing sea urchins. Journal of Evolutionary Biology, 1, 27–44.

    Article  Google Scholar 

  • Parzer, H. F., & Moczek, A. P. (2008). Rapid antagonistic coevolution between primary and secondary sexual characters in horned beetles. Evolution, 62, 2423–2428.

    Article  PubMed  Google Scholar 

  • Pfennig, D. W., & McGee, M. (2010). Resource polyphenism increases species richness: A test of the hypothesis. Philosophical Transactions of the Royal Society Series B, 365, 577–591.

    Article  Google Scholar 

  • Pfennig, D. W., Wund, M. A., Snell-Rood, E. C., Cruickshank, T., Schlichting, C. D., & Moczek, A. P. (2010). Phenotypic plasticity’s impacts on diversification and speciation. Trends in Ecology & Evolution, 25, 459–467.

    Article  Google Scholar 

  • Pigeon, D., Chouinard, A., & Bernatchez, L. (1997). Multiple modes of speciation involved in the parallel evolution of sympatric morphotypes of lake whitefish (Coregonus clupeaformis, Salmonidae). Evolution, 51, 196–205.

    Article  Google Scholar 

  • Pigliucci, M. (2001). Phenotypic plasticity: Beyond nature and nurture. Baltimore, MD: The Johns Hopkins University Press.

    Google Scholar 

  • Pigliucci, M. (2008). Is evolvability evolvable? Nature Reviews Genetics, 9, 75–82.

    Article  PubMed  CAS  Google Scholar 

  • Pigliucci, M., & Müller, G. B. (Eds.). (2010). Evolution: The extended synthesis. Cambridge, MA: MIT Press.

    Google Scholar 

  • Pors, B., & Werner, P. A. (1989). Individual flowering time in a goldenrod (Solidago canadensis). Field experiments show genotype more important than environment. American Journal of Botany, 76, 1681–1688.

    Article  Google Scholar 

  • Porter, A. H., & Johnson, N. A. (2002). Speciation despite gene flow when developmental pathways evolve. Evolution, 56, 2103–2111.

    PubMed  Google Scholar 

  • Prtichard, N. M., & Tutin, T. G. (1972). Gentianella Moench. In T. G. Tutin, V. H. Heywood, N. A. Burges, D. M. Moore, D. H. Valentine, S. M. Walters, & D. A. Webb (Eds.), Flora Europaea (Vol. 3, pp. 63–67). Cambridge: Cambridge University Press.

    Google Scholar 

  • Prud’homme, B., Minervino, C., Hocine, M., Cande, J. D., Aouane, A., Dufour, H. D., et al. (2011). Body plan innovation in treehoppers through the evolution of an extra wing-like appendage. Nature, 473, 83–86.

    Article  PubMed  CAS  Google Scholar 

  • Raff, R. A. (1992). Direct-developing sea urchins and the evolutionary reorganization of early development. BioEssays, 14, 211–218.

    Article  PubMed  CAS  Google Scholar 

  • Renaut, S., & Bernatchez, L. (2011). Transcriptome-wide signature of hybrid breakdown associated with intrinsic reproductive isolation in lake whitefish species pairs (Coregonus spp., Salmonidae). Heredity, 106, 1003–1011.

    Article  PubMed  CAS  Google Scholar 

  • Rice, S. H. (2004). Evolutionary theory: Mathematical and conceptual foundations. Sunderland MA: Sinauer.

    Google Scholar 

  • Rogers, S. M., & Bernatchez, L. (2006). The genetic basis of intrinsic and extrinsic postzygotic reproductive isolation jointly promoting speciation in the lake whitefish species complex (Coregonus clupeaformis). Journal of Evolutionary Biology, 19, 1979–1994.

    Article  PubMed  CAS  Google Scholar 

  • Rundle, H. D., & Nosil, P. (2005). Ecological speciation. Ecology Letters, 8, 336–352.

    Article  Google Scholar 

  • Saint-Laurent, R., Legault, M., & Bernatchez, L. (2003). Divergent selection maintains adaptive differentiation despite high gene flow between sympatric rainbow smelt ecotypes (Osmerus mordax Mitchill). Molecular Ecology, 12, 315–330.

    Article  PubMed  CAS  Google Scholar 

  • Scannell, D. R., Byrne, K. P., Gordon, J. L., Wong, S., & Wolfe, K. H. (2006). Multiple rounds of speciation associated with reciprocal gene loss in polyploid yeasts. Nature, 440, 341–345.

    Article  PubMed  CAS  Google Scholar 

  • Schluter, D. (2000). The ecology of adaptive radiation. Oxford, UK: Oxford University Press.

    Google Scholar 

  • Schluter, D., & McPhail, J. D. (1993). Character displacement and replicate adaptive radiation. Trends in Ecology & Evolution, 8, 197–200.

    Article  CAS  Google Scholar 

  • Scott, D. E. (1993). Timing of reproduction of paedomorphic and metamorphic Ambystoma talpoideum. American Midland Naturalist, 129, 397–402.

    Article  Google Scholar 

  • Semlitch, R. D., & Wilbur, H. M. (1989). Artificial selection for paedomorphosis in the salamander Ambystoma talpoideum. Evolution, 43, 105–112.

    Article  Google Scholar 

  • Semon, M., & Wolfe, K. H. (2007a). Consequences of genome duplication. Current Opinion in Genetics & Development, 17, 505–512.

    Article  CAS  Google Scholar 

  • Semon, M., & Wolfe, K. H. (2007b). Reciprocal gene loss between Tetraodon and zebrafish after whole genome duplication in their ancestor. Trends in Genetics, 23, 108–112.

    Article  PubMed  CAS  Google Scholar 

  • Simpson, G. G. (1944). Tempo and mode in evolution. New York, NY: Columbia University Press.

    Google Scholar 

  • Simpson, G. G. (1953). The major features of evolution. New York, NY: Columbia University Press.

    Google Scholar 

  • Skúlason, S., Snorrason, S. S., & Jónsson, B. (1999). Sympatric morphs, populations and speciation in freshwater fish with emphasis on arctic charr. In A. E. Magurran & R. M. May (Eds.), Evolution of biological diversity (pp. 70–92). Oxford: Oxford University Press.

    Google Scholar 

  • Smith, T. B., & Skúlason, S. (1996). Evolutionary significance of resource polymorphisms in fishes, amphibians, and birds. Annual Reviews in Ecology and Systematics, 27, 111–133.

    Article  Google Scholar 

  • Snell-Rood, E. C., Cash, A., Han, M. V., Kijimoto, T., Andrews, A., & Moczek, A. P. (2011). Developmental decoupling of alternative phenotypes: insights from the transcriptomes of horn-polyphenic beetles. Evolution, 65, 231–245.

    Article  PubMed  Google Scholar 

  • Tauber, M. J., Tauber, C. A., & Masaki, S. I. (1986). Seasonal adaptations of insects. Oxford: Oxford University Press.

    Google Scholar 

  • Tauber, C. A., Tauber, M. J., & Nechols, J. R. (1977). Two genes control seasonal isolation in sibling species. Science, 197, 592–593.

    Article  PubMed  CAS  Google Scholar 

  • Taylor, E. B., & Bentzen, P. (1993). Evidence for multiple origins and sympatric divergence of trophic ecotypes of smelt (Osmerus) in Northeastern North America. Evolution, 47, 813–832.

    Article  Google Scholar 

  • The Marie Curie SPECIATION Network. (2012). What do we need to know about speciation? Trends in Ecology & Evolution, 27, 27–39.

    Article  Google Scholar 

  • Tills, O., Rundle, S. D., Salinger, M., Haun, T., Pfenninger, M., & Spicer, J. I. (2011). A genetic basis for intraspecific differences in developmental timing? Evolution & Development, 13, 542–548.

    Article  Google Scholar 

  • von Wettstein, R. (1895). Der Saison-Dimorphismus als Ausgangspunkt für die Bildung neuer Arten im Pflanzenreich. Berichte der Deutschen botanischen Gesellschaft, 13, 303–313.

    Google Scholar 

  • Wagner, A. (2011). The origins of evolutionary innovations. Oxford: Oxford University Press.

    Google Scholar 

  • Wagner, G. P., Amemiya, C., & Ruddle, F. (2003). Hox cluster duplications and the opportunity for evolutionary novelties. Proceedings of the National Academy of Sciences of the United States of America, 100, 14603–14606.

    Article  PubMed  CAS  Google Scholar 

  • Wagner, G. P., & Draghi, J. (2010). Evolution and evolvability. In M. Pigliucci & G. B. Müller (Eds.), Evolution: The extended synthesis (pp. 379–399). Cambridge, MA: MIT Press.

    Google Scholar 

  • Wagner, G. P., & Zhang, J. (2011). The pleiotropic structure of the genotype–phenotype map: The evolvability of complex organisms. Nature Reviews Genetics, 12, 204–213.

    Article  PubMed  CAS  Google Scholar 

  • Wasik, B., & Moczek, A. P. (2011). decapentaplegic (dpp) regulates the growth of a morphological novelty, beetle horns. Development Genes and Evolution, 221, 17–27.

    Article  PubMed  Google Scholar 

  • Wasik, B. R., & Moczek, A. P. (in press). pangolin expression influences the development of a morphological novelty: Beetle horns. Genesis,. doi:10.1002/dvg.20814.

  • Wasik, B. R., Rose, D. J., & Moczek, A. P. (2010). Beetle horns are regulated by the Hox gene, Sex combs reduced, in a species- and sex-specific manner. Evolution & Development, 12, 353–362.

    Article  CAS  Google Scholar 

  • West-Eberhard, M. J. (1986). Alternative adaptations, speciation and phylogeny (a review). Proceedings of the National Academy of Sciences of the United States of America, 83, 1388–1392.

    Article  PubMed  CAS  Google Scholar 

  • West-Eberhard, M. J. (1989). Phenotypic plasticity and the origin of diversity. Annual Reviews of Ecology and Systematics, 20, 249–278.

    Article  Google Scholar 

  • West-Eberhard, M. J. (2003). Developmental plasticity and evolution. Oxford: Oxford University Press.

    Google Scholar 

  • West-Eberhard, M. J. (2005). Developmental plasticity and the origin of species differences. Proceedings of the National Academy of Sciences of the United States of America, 102(Supplement 1), 6543–6549.

    Article  PubMed  CAS  Google Scholar 

  • Williams, K. S., & Simon, C. (1995). The ecology, behavior, and evolution of periodical cicadas. Annual Reviews of Entomology, 40, 269–295.

    Article  CAS  Google Scholar 

  • Wray, G. A. (2010). Integrating genomics into evolutionary theory. In M. Pigliucci & G. B. Müller (Eds.), Evolution: The extended synthesis (pp. 97–116). Cambridge, MA: MIT Press.

    Google Scholar 

  • Yoshizawa, K. (2012). The treehopper’s helmet is not homologous with wings (Hemiptera: Membracidae). Systematic Entomology, 37, 2–6.

    Article  Google Scholar 

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Acknowledgments

We are grateful to Maria Pia Miglietta, Francesco Santini and Anuschka Faucci for their kind invitation to contribute to this issue on speciation from the perspective of evolutionary developmental biology. Insightful comments from two anonymous referees on a previous version substantially contributed to the improvement of our ms. Mark Epstein has kindly contributed precious linguistic advice.

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Correspondence to Giuseppe Fusco.

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Minelli, A., Fusco, G. On the Evolutionary Developmental Biology of Speciation. Evol Biol 39, 242–254 (2012). https://doi.org/10.1007/s11692-012-9175-6

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