Biological Systematics in the Evo-Devo era

  • Alessandro Minelli University of Padova, Department of Biology, Via Ugo Bassi 58 B, I -35131 Padova
Keywords: genotype→phenotype map, heterochrony, saltational evolution, speciation, temporal phenotype

Abstract

Evolutionary developmental biology (evo-devo) suggests a distinction between modular and systemic variation. In the case of modular change, the conservation of the overall structure helps recognizing affinities, while a single, fast evolving module is likely to produce a bonanza for the taxonomist, while systemic changes produce strongly deviating morphologies that cause problems in tracing homologies. Similarly, changes affecting the whole life cycle are more challenging than those limited to one stage. Developmental modularity is a precondition for heterochrony. Analyzing a matrix of morphological data for paedomorphic taxa requires special care. It is, however, possible to extract phylogenetic signal from heterochronic patterns. The taxonomist should pay attention to the intricacies of the genotype→phenotype map. When using genetic data to infer phylogeny, a comparison of gene sequences is just a first step. To bridge the gap between genes and morphology we should consider the spatial and temporal patterns of gene expression, and their regulation. Minor genetic change can have major phenotypic effects, sometimes suggesting saltational evolution. Evo-devo is also relevant in respect to speciation: changes in developmental schedules are often implicated in the divergence between sympatric morphs, and a developmental modulation of ‘temporal phenotypes’ appears to be responsible for many cases of speciation.

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. http://dx.doi.org/10.1038/nature04843

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. http://dx.doi.org/10.1126/science.1098095

Alberch P. 1991. From genes to phenotype: dynamical systems and evolvability. Genetica 84: 5–11. http://dx.doi.org/10.1007/BF00123979

Alberch P., Gould S.J., Oster G. & Wake D. 1979. Size and shape in ontogeny and phylogeny. Paleobiology 5: 296–317.

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

Alexander R.D. & Bigelow R.S. 1960. Allochronic speciation in field crickets, and a new species, Acheta veletis. Evolution 14: 334–346. http://dx.doi.org/10.2307/2405976

Allsopp P.G. & Lambkin C.L. 2006. Canegrubs and cladistics: what story do adult, larval and ecological characters tell? Australian Journal of Entomology 45: 55–66. http://dx.doi.org/10.1111/j.1440-6055.2006.00511.x

Altenberg L. 1995. Genome growth and the evolution of the genotype-phenotype map. In: Banzhaf W. & Eeckman F.H. (eds) Evolution and Biocomputation. Computational Models of Evolution: 205–259. Springer, Berlin.

Amundson R. 2005. The Changing Role of the Embryo in Evolutionary Thought: Roots of Evo-Devo. Cambridge University Press, Cambridge.

Angelini D.R. & Kaufman T.C. 2005. Comparative developmental genetics and the evolution of arthropod body plans. Annual Review of Genetics 39: 95–119. http://dx.doi.org/10.1146/annurev.genet.39.073003.112310

Arthur W. 2002. The emerging conceptual framework of evolutionary developmental biology. Nature 415: 757–764. http://dx.doi.org/10.1038/415757a

Balavoine G., de Rosa R. & Adoutte A. 2002. Hox clusters and bilaterian phylogeny. Molecular Phylogenetics and Evolution 24: 366–373. http://dx.doi.org/10.1016/S1055-7903(02)00237-3

Bely A.E. & Weisblat D.A. 2006. Lessons from leeches: a call for DNA barcoding in the lab. Evolution & Development 8: 491–501. http://dx.doi.org/10.1111/j.1525-142X.2006.00122.x

Beutel R.G. & Leschen R.A.B. 2005. Phylogenetic analysis of Staphyliniformia (Coleoptera) based on characters of larvae and adults. Systematic Entomology 30: 510–548. http://dx.doi.org/10.1111/j.1365-3113.2005.00293.x

Bininda-Emonds O.R.P., Jeffery J.E., Coates M.I. & Richardson M.K. 2002. From Haeckel to event-pairing: the evolution of developmental sequences. Theory in Biosciences 121: 297–320. http://dx.doi.org/10.1007/s12064-002-0016-5

Bininda-Emonds O.R.P., Jeffery J.E., Sánchez-Villagra M.R., Hanken J., Colbert M., Pieau C., Selwood L., Ten Cate C., Raynaud A., Osabutey C. & Richardson M.K. 2007. Forelimb-hindlimb developmental timing across tetrapods. BMC Evolutionary Biology 7: 182. http://dx.doi.org/10.1186/1471-2148-7-182

Blomquist G.E. 2008. Methods of sequence heterochrony for describing modular developmental changes in human evolution. American Journal of Physical Anthropology 138: 231–238. http://dx.doi.org/10.1002/ajpa.20963

Bonner J.T. 1988. The Evolution of Complexity. Princeton Univ. Press, Princeton, NJ.

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. http://dx.doi.org/10.1111/j.1095-8339.2008.00794.x

Boyden A. & Shelswell E.M. 1959. Prophylogeny: some considerations regarding primitive evolution in lower Metazoa. Acta Biotheoretica 13: 115–130. http://dx.doi.org/10.1007/BF01556648

Briggs D. & Walters S.M. 1997. Plant Variation and Evolution. 3rd ed., Cambridge University Press, Cambridge.

Brooks D.R. & McLennan D.A. 1993. Macroevolutionary patterns of morphological diversification among parasitic flatworms (Platyhelminthes: Cercomeria). Evolution 47: 495–509. http://dx.doi.org/10.2307/2410067

Brunetti C.R., Selegue J.E., Monteiro A., French V., Brakefield P.M. & Carroll S.B. 2001. The generation and diversification of butterfly eyespot color patterns. Current Biology 11: 1578–1585. http://dx.doi.org/10.1016/S0960-9822(01)00502-4

Carlquist S. 1974. Island Biology. Columbia University Press, New York, NY.

Carlquist S. 1980. Hawaii. A Natural History. 2nd ed., Pacific Tropical Botanical Garden, Kauai, Hawaii.

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.

Chen T.C., Zhang D.X., Larsen K., Larsen S.S. 2010. Bauhinia Linnaeus. In: Wu Z.Y., Raven P.H. & Hong D.Y. (eds) Flora of China, 10: 6–21. Science Press, Beijing & Missouri Botanical Garden Press, St. Louis, MO.

Citerne H.L., Pennington R.T. & Cronk Q.C.B. 2006. An apparent reversal in floral symmetry in the legume Cadia is a homeotic transformation. Proceedings of the National Academy of Sciences of the United States of America 103: 12017–12020. http://dx.doi.org/10.1073/pnas.0600986103

Cook C.E., Smith M.L., Telford M.J., Bastianello A. & Akam M. 2001. Hox genes and the phylogeny of the arthropods. Current Biology 11: 759–763. http://dx.doi.org/10.1016/S0960-9822(01)00222-6

Copf T., Rabet N., Celniker S.E. & Averof M. 2003. Posterior patterning genes and the identification of a unique body region in the brine shrimp Artemia franciscana. Development 130: 5915–5927. http://dx.doi.org/10.1242/dev.00835

Cracraft J. 2005. Phylogeny and evo-devo: characters, phylogeny and historical analysis of the evolution of development. Zoology 108: 345–356. http://dx.doi.org/10.1016/j.zool.2005.09.003

Cunningham C. 1999. Some limitations of ancestral character-state reconstruction when testing evolutionary hypotheses. Systematic Biology 48: 665–674. http://dx.doi.org/10.1080/106351599260238

Cuvier G. 1812. Recherches sur les ossements fossiles de quadrupèdes, où l’on rétablit les caractères de plusieurs espèces d’animaux que les révolutions du globe paraissent avoir détruites, 4 volumes. Deterville, Paris.

Darwin C. 1859. On the Origin of Species by Natural Selection, or the Preservation of Favoured Races in the Struggle for Life. John Murray, London. http://www.biodiversitylibrary.org/bibliography/87916#/summary

de Beer G.R. 1930. Embryology and Evolution. Clarendon Press, Oxford.

de Beer G.R. 1940. Embryos and Ancestors. Clarendon Press, Oxford.

de Jong I.M.L., Colbert M.W., Witte F. & Richardson M.K. 2009. Polymorphism in developmental timing: intraspecific heterochrony in a Lake Victoria cichlid. Evolution & Development 11: 625–635. http://dx.doi.org/10.1111/j.1525-142X.2009.00370.x

de Rosa R., Grenier J.K., Andreeva T., Cook C.E., Adoutte A., Akam M., Carroll S.B. & Balavoine G. 1999. Hox genes in brachiopods and priapulids and protostome evolution. Nature 399: 772–776.

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

Dehal P., Satou Y., Campbell R.K., Chapman J., Degnan B., De Tomaso A., Davidson B., Di Gregorio A., Gelpke M., Goodstein D.M., Harafuji N., Hastings K.E., Ho I., Hotta K., Huang W., Kawashima T., Lemaire P., Martinez D., Meinertzhagen I.A., Necula S., Nonaka M., Putnam N., Rash S., Saiga H., Satake M., Terry A., Yamada L., Wang H.G., Awazu S., Azumi K., Boore J., Branno M., Chin-Bow S., DeSantis R., Doyle S., Francino P., Keys D.N., Haga S., Hayashi H., Hino K., Imai K.S., Inaba K., Kano S., Kobayashi K., Kobayashi M., Lee B.I., Makabe K.W., Manohar C., Matassi G., Medina M., Mochizuki Y., Mount S., Morishita T., Miura S., Nakayama A., Nishizaka S., Nomoto H., Ohta F., Oishi K., Rigoutsos I., Sano M., Sasaki A., Sasakura Y., Shoguchi E., Shin-i T., Spagnuolo A., Stainier D., Suzuki MM., Tassy O., Takatori N., Tokuoka M., Yagi K., Yoshizaki F., Wada S., Zhang C., Hyatt PD., Larimer F., Detter C., Doggett N., Glavina T., Hawkins T., Richardson P., Lucas S., Kohara Y., Levine M., Satoh N. & Rokhsar D.S. 2002. The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298: 2157–2167. http://dx.doi.org/10.1126/science.1080049

Dollo L. 1893. Les lois de l’évolution. Bulletin de la Société belge de Géologie, de Paléontologie et d’Hydrologie 7: 164–166.

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.

Drago L., Fusco G., Garollo E. & Minelli A. 2011. Structural aspects of leg-to-gonopod metamorphosis in male helminthomorph millipedes (Diplopoda). Frontiers in Zoology 8: 19. http://dx.doi.org/10.1186/1742-9994-8-19

Drago L., Fusco G. & Minelli A. 2008. Non-systemic metamorphosis in male millipede appendages: long delayed, reversible effect of an early localized positional marker? Frontiers in Zoology 5: 5. http://dx.doi.org/10.1186/1742-9994-5-5

Duboule D. 1994. Temporal colinearity and the phylotypic progression: a basis for the stability of a vertebrate Bauplan and the evolution of morphologies through heterochrony. Development Suppl.: 135–142.

Fišer C., Bininda-Emonds O.R.P., Blejec A., & Sket B. 2008. Can heterochrony help explain the high morphological diversity within the genus Niphargus (Crustacea: Amphipoda)? Organisms Diversity and Evolution 8: 146–162. http://dx.doi.org/10.1016/j.ode.2007.06.002

Flohr R.C.E., Blom C.J., Rainey P.B. & Beaumont H.J.E. 2013. Founder niche constrains evolutionary adaptive radiation. Proceedings of the National Academy of Sciences of the United States of America 110: 20663–20668. http://dx.doi.org/10.1073/pnas.1310310110

Frazzetta T.H. 2012. Flatfishes, turtles, and bolyerine snakes: evolution by small steps or large, or both? Evolutionary Biology 39: 30–60. http://dx.doi.org/10.1007/s11692-011-9142-7

Gao K.-Q. & Shubin N.H. 2001. Late Jurassic salamanders from northern China. Nature 410: 574–577. http://dx.doi.org/10.1038/35069051

Giribet G., Sørensen M.V., Funch P., Kristensen R.M. & Sterrer W. 2004. Investigations into the phylogenetic position of Micrognathozoa using four molecular loci. Cladistics 20: 1–13. http://dx.doi.org/10.1111/j.1096-0031.2004.00004.x

Givnish T.J., Millam K.C., Mast A.R., Paterson T.B., Theim T.J., Hipp A.L., Henss J.M., Smith J.F., Wood K.R. & Sytsma K.J. 2009. Origin, adaptive radiation and diversification of the Hawaiian lobeliads (Asterales: Campanulaceae). Proceedings of the Royal Society of London, Series B, Biological Sciences 276: 407–416. http://dx.doi.org/10.1098/rspb.2008.1204

Glenner H., Høeg J.T., Grygier M.J. & Fujita Y. 2008. Induced metamorphosis in crustacean y-larvae: Towards a solution to a 100-year-old riddle. BMC Biology 6: 21. http://dx.doi.org/10.1186/1741-7007-6-21

Goldschmidt R. 1940. The Material Basis of Evolution. Yale University Press, New Haven, CT.

Goswami A. 2007. Cranial modularity and sequence heterochrony in mammals. Evolution & Development 9: 290–298. http://dx.doi.org/10.1111/j.1525-142X.2007.00161.x

Gould S.J. 1977. Ontogeny and Phylogeny. The Belknap Press of Harvard University Press, Cambridge, MA.

Grimes J. 1999. Inflorescence morphology, heterochrony, and phylogeny in the mimosoid tribes Ingeae and Acacieae (Leguminosae: Mimosoideae). Botanical Review 65: 317–347. http://dx.doi.org/10.1007/BF02857753

Guerrant E.O.J. 1982. Neotenic evolution of Delphinium nudicaule (Ranunculaceae), a humming-bird pollinated larkspur. Evolution 36: 699–712. http://dx.doi.org/10.2307/2407883

Guralnick R.P. & Lindberg D.R. 2001. Reconnecting cell and animal lineages: what do cell lineages tell us about the evolution and development of Spiralia? Evolution 55: 1501–1519. http://dx.doi.org/10.1111/j.0014-3820.2001.tb00671.x

Haeckel E. 1866. Generelle Morphologie der Organismen. Allgemeine Grundzüge der organischen Formen-Wissenschaft, mechanisch begründet durch die von Charles Darwin reformirte Descendenz-Theorie. Reimer, Berlin. http://www.biodiversitylibrary.org/bibliography/101747#/summary

Hall B.K. 1992. Evolutionary Developmental Biology. Chapman & Hall, London.

Hall B.K. 1998. Evolutionary Developmental Biology. Second Edition, Chapman & Hall, London.

Hall B.K. & Olson W.M. 2003. Keywords and Concepts in Evolutionary Developmental Biology. Harvard University Press, Cambridge, MA & London.

Harrison L. & Larsson H. 2008. Estimating evolution of temporal sequence changes: a practical approach to inferring ancestral developmental sequences and sequence heterochrony. Systematic Biology 57: 378–387. http://dx.doi.org/10.1080/10635150802164421

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. http://dx.doi.org/10.1111/j.1601-5223.1988.tb00178.x

Hendrikse J.L., Parsons T.E. & Hallgrímsson B. 2007. Evolvability as the proper focus of evolutionary developmental biology. Evolution & Development 9: 393–401. http://dx.doi.org/10.1111/j.1525-142X.2007.00176.x

Hennig W. 1966. Phylogenetic Systematics. University of Illinois Press, Urbana, IL.

Henriquez C.L., Arias T., Pires J.C., Croat T.B. & Schaal B.A. 2014. Phylogenomics of the plant family Araceae. Molecular Phylogenetics and Evolution 75: 91–102. http://dx.doi.org/10.1016/j.ympev.2014.02.017

Hilu K.W. 1983. The role of single-gene mutations in the evolution of flowering plants. Evolutionary Biology 16: 97–128.

Hueber S.D., Rauch J., Djordjevic M.A., Gunter H., Weiller G.F. & Frickey T. 2013. Analysis of central Hox protein types across bilaterian clades: on the diversification of central Hox proteins from an Antennapedia/Hox7-like protein. Developmental Biology 383: 175–185. http://dx.doi.org/10.1016/j.ydbio.2013.09.009

Hughes C.L & Kaufman T.C. 2002. Hox genes and the evolution of the arthropod body plan. Evolution & Development 4: 459–499. http://dx.doi.org/10.1046/j.1525-142X.2002.02034.x

Iannelli F., Pesole G., Sordino P. & Gissi C. 2007. Mitogenomics reveals two cryptic species in Ciona intestinalis. Trends in Genetics 23: 419–422. http://dx.doi.org/10.1016/j.tig.2007.07.001

Jager M., Murienne J., Clabaut C., Deutsch J., Le Guyader H. & Manuel M. 2006. Homology of arthropod anterior appendages revealed by Hox gene expression in a sea spider. Nature 441: 506–508. http://dx.doi.org/10.1038/nature04591

Janssen R., Eriksson B.J., Tait N.N. & Budd G.E. 2014. Onychophoran Hox genes and the evolution of arthropod Hox gene expression. Frontiers in Zoology 11: 22. http://dx.doi.org/10.1186/1742-9994-11-22

Jeffery J.E., Bininda-Emonds O.R.P., Coates M.I. & Richardson M.K. 2005. A new technique for identifying sequence heterochrony. Systematic Biology 54: 230–240. http://dx.doi.org/10.1080/10635150590923227

Jenner R.A. 2006. Unburdening evo-devo: ancestral attractions, model organisms, and basal baloney. Development Genes and Evolution 216: 385–394. http://dx.doi.org/10.1007/s00427-006-0084-5

Judd D.D. 1998. Exploring component stability using life-stage concordance in sabethine mosquitoes (Diptera: Culicidae). Cladistics 14: 63–93. http://dx.doi.org/10.1111/j.1096-0031.1998.tb00204.x

Kim J., Kerr J.Q. & Min G.-S. 2000. Molecular heterochrony in the early development of Drosophila. Proceedings of the National Academy of Sciences of the United States of America 97: 212–216. http://dx.doi.org/10.1073/pnas.97.1.212

Kim K., Kotov A.A. & Taylor D.J. 2006. Hormonal induction of undescribed males resolves cryptic species of cladocerans. Proceedings of the Royal Society of London B 273: 141–147. http://dx.doi.org/10.1098/rspb.2005.3299

Klingenberg C.P. 1998. Heterochrony and allometry: the analysis of evolutionary change in ontogeny. Biological Reviews 73: 79–123. http://dx.doi.org/10.1111/j.1469-185X.1997.tb00026.x

Klingenberg C.P. 2005. Developmental constraints, modules and evolvability. In: Hallgrímsson B. & Hall B. K. (eds) Variation: A Central Concept in Biology: 219–247. Elsevier, Burlington, MA.

Kowalewski A. 1866. Entwicklungsgeschichte der einfachen Ascidien. Mémoires de l’Académie Impériale des Sciences de St. Petersbourg (7)10: 1–119.

Kutschera U., Langguth H., Kuo D.-H., Weisblat D.A. & Shankland M. 2013. Description of a new leech species from North America, Helobdella austinensis n. sp. (Hirudinea: Glossiphoniidae), with observations on its feeding behaviour. Zoosystematics and Evolution 89: 239–246. http://dx.doi.org/10.1002/zoos.201300010

Lammers T.G. 1990. Campanulaceae. In: Wagner W.L., Herbst D.R. & Sohmer S.H. (eds) Manual of the Flowering Plants of Hawai’i: 420–489. University of Hawaii Press, Honolulu, Hawaii.

Landry L., Vincent W.F. & Bernatchez L. 2007. Parallel evolution of lake whitefish dwarf ecotypes in association with limnological features of their adaptive landscape. Journal of Evolutionary Biology 20: 971–984. http://dx.doi.org/10.1111/j.1420-9101.2007.01304.x

Lennartsson T. 1997. Seasonal differentiation—a conservative reproductive barrier in two grassland Gentianella (Gentianaceae) species. Plant Systematics and Evolution 208: 45–69. http://dx.doi.org/10.1007/BF00986082

Li P. & Johnston M.O. 2010. Flower development and the evolution of self-fertilization in Amsinckia: the role of heterochrony. Evolutionary Biology 37: 143–168. http://dx.doi.org/10.1007/s11692-010-9091-6

Manuel M., Jager M., Murienne J., Clabaut C. & Le Guyader H. 2006. Hox genes in sea spiders (Pycnogonida) and the homology of arthropod head segments. Development Genes and Evolution 216: 481–491. http://dx.doi.org/10.1007/s00427-006-0095-2

Marcellini S. & Simpson P. 2006. Two or four bristles: functional evolution of an enhancer of scute in Drosophilidae. PLoS Biology 4 (12): e386. http://dx.doi.org/10.1371/journal.pbio.0040386

Marshall D.C. & Cooley J.R. 2000. Reproductive character displacement and speciation of a new species, 13-year Magicicada neotredecim. Evolution 54: 1313–1325. http://dx.doi.org/10.1111/j.0014-3820.2000.tb00564.x

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. http://dx.doi.org/10.1603/AN10087

McKinney M.L. (ed.) 1988. Heterochrony in Evolution: A Multidisciplinary Approach. Plenum, New York-London.

McKinney M.L. & McNamara K.J. 1991. Heterochrony. The Evolution of Ontogeny. Plenum, New York-London.

McNamara K.J. 1986. A guide to the nomenclature of heterochrony. Journal of Paleontology 60: 4–13.

McNamara K.J. (ed.) 1995. Evolutionary Change and Heterochrony. Wiley, Chichester.

McShea D.W. 2000. Functional complexity in organisms: parts as proxies. Biology and Philosophy 15: 641–668. http://dx.doi.org/10.1023/A:1006695908715

Meier R. 1996. Larval morphology of the Sepsidae (Diptera: Sciomyzoidea), with a cladistic analysis using adult and larval characters. Bulletin of the American Museum of Natural History 228: 1–147.

Meier R. & Lim G.S. 2009. Conflict, convergent evolution, and the relative importance of immature and adult characters in endopterygote phylogenetics. Annual Review of Entomology 54: 85–104. http://dx.doi.org/10.1146/annurev.ento.54.110807.090459

Minelli A. 2007. Invertebrate taxonomy and evolutionary developmental biology. Zootaxa 1668: 55–60.

Minelli A. 2009. Perspectives in Animal Phylogeny and Evolution. Oxford University Press, Oxford.

Minelli A. 2011. Animal development, an open-ended segment of life. Biological Theory 6: 4–15. http://dx.doi.org/10.1007/s13752-011-0002-6

Minelli A. 2014. Developmental disparity. In: Minelli A. & Pradeu T. (eds) Towards a Theory of Development: 227–245. Oxford University Press, Oxford.

Minelli A. 2015. Morphological misfits and the architecture of development. In: Serrelli E. & Gontier N. (eds) Macroevolution. Explanation, Interpretation and Evidence: 329–343. Springer, Cham, Switzerland. http://dx.doi.org/10.1007/978-3-319-15045-1_10

Minelli A. in press. Evo Devo and its significance for animal evolution and phylogeny. In: Wanninger A. (ed.) Evolutionary Developmental Biology of Invertebrates 1: Introduction, Non-Bilateria, Acoelomorpha, Xenoturbellida, Chaetognatha. Springer, Vienna.

Minelli A. & Baedke J. 2014. Model organisms in evo-devo: promises and pitfalls of the comparative approach. History and Philosophy of the Life Sciences 36: 42–59. http://dx.doi.org/10.1007/s40656-014-0004-3

Minelli A. & Fusco G. 2012. On the evolutionary developmental biology of speciation. Evolutionary Biology 39: 242–254. http://dx.doi.org/10.1007/s11692-012-9175-6

Minelli A. & Pradeu T. 2014. Towards a Theory of Development. Oxford University Press, Oxford.

Minelli A., Chagas A.J. & Edgecombe G.D. 2009. Saltational evolution of trunk segment number in centipedes. Evolution & Development 11: 318–322. http://dx.doi.org/10.1111/j.1525-142X.2009.00334.x

Minelli A., Negrisolo E. & Fusco G. 2007. Reconstructing animal phylogeny in the light of evolutionary developmental biology. In: Hodkinson T.R. & Parnell J.A.N. (eds) Reconstructing the Tree of Life: Taxonomy and Systematics of Species Rich Taxa: 177–190. Taylor and Francis - CRC Press, Boca Raton, FL.

Müller G.B. 2008. Evo-devo as a discipline. In: Minelli A. & Fusco G. (eds) Evolving Pathways. Key Themes in Evolutionary Developmental Biology: 5–30. Cambridge University Press, Cambridge.

Naiki A. 2012. Heterostyly and the possibility of its breakdown by polyploidization. Plant Species Biology 27: 3–29. http://dx.doi.org/10.1111/j.1442-1984.2011.00363.x

Naisbit R.E., Jiggins C.D. & Mallet J. 2003. Mimicry: developmental genes that contribute to speciation. Evolution & Development 5: 269–280. http://dx.doi.org/10.1046/j.1525-142X.2003.03034.x

Neves R.C., Kristensen R.M. & Funch P. 2012. Ultrastructure and morphology of the cycliophoran female. Journal of Morphology 273: 850–869. http://dx.doi.org/10.1002/jmor.20025

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. http://dx.doi.org/10.1186/1471-2148-9-59

Obst M. & Funch P. 2003. Dwarf male of Symbion pandora (Cycliophora). Journal of Morphology 255: 261–278. http://dx.doi.org/10.1002/jmor.10040

Oosterbroek P. & Courtney G. 1995. Phylogeny of the nematocerous families of Diptera (Insecta). Zoological Journal of the Linnean Society 115: 267–311. http://dx.doi.org/10.1006/zjls.1995.0080

Orr H.A. 1998. The population genetics of adaptation: the distribution of factors fixed during adaptive evolution. Evolution 52: 935–949. http://dx.doi.org/10.2307/2411226

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. http://dx.doi.org/10.1111/j.1420-9101.2004.00844.x

Passamaneck Y.J. & Halanych K.M. 2004. Evidence from Hox genes that bryozoans are lophotrochozoans. Evolution & Development 6: 275–281. http://dx.doi.org/10.1111/j.1525-142X.2004.04032.x

Penz C.M., Freitas A.V.L., Kaminski L.A., Casagrande M.M. & Devries P.J. 2013. Adult and early-stage characters of Brassolini contain conflicting phylogenetic signal (Lepidoptera, Nymphalidae). Systematic Entomology 38: 316–333. http://dx.doi.org/10.1111/syen.12000

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. http://dx.doi.org/10.2307/2410973

Pigliucci M. 2010. Genotype–phenotype mapping and the end of the ‘genes as blueprint’ metaphor. Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences 365: 557–566. http://dx.doi.org/10.1098/rstb.2009.0241

Pigliucci M. & Müller G. (eds) 2010. Evolution: The Extended Synthesis. MIT Press, Cambridge, MA.

Pistillo D., Skaer N. & Simpson P. 2002. scute expression in C. vicina reveals an ancestral pattern of longitudinal stripes on the thorax of higher Diptera. Development 129: 563–572.

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. http://dx.doi.org/10.2307/2444406

Prenner G. & Klitgaard B.B. 2008. Towards unlocking the deep nodes of Leguminosae: floral development and morphology of the enigmatic Duparquetia orchidacea (Leguminosae, Caesalpinioideae). American Journal of Botany 95: 1349–1365. http://dx.doi.org/10.3732/ajb.0800199

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

Raff R.A. & Kaufman T.C. 1983. Embryos, Genes, and Evolution. Macmillan, New York.

Remane A. 1952. Die Grundlagen des natürlichen Systems der vergleichenden Anatomie und der Phylogenetik. Geest & Portig, Leipzig.

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. http://dx.doi.org/10.1038/hdy.2010.149

Richardson M.K. 1995. Heterochrony and the phylotypic period. Developmental Biology 172: 412–421. http://dx.doi.org/10.1006/dbio.1995.8041

Richardson M.K., Hanken J., Gooneratne M.L., Pieau C., Raynaud A., Selwood L. & Wright G.M. 1997. There is no highly conserved embryonic stage in the vertebrates: implications for current theories of evolution and development. Anatomy & Embryology 196: 91–106. http://dx.doi.org/10.1007/s004290050082

Richardson M.K., Jeffery J.E., Coates M.I. & Bininda-Emonds O.R.P. 2001. Comparative methods in developmental biology. Zoology 104: 278–283. http://dx.doi.org/10.1078/0944-2006-00033

Rogers S.M. & Bernatchez L. 2006. The genetic basis of intrinsic and extrinsic post-zygotic reproductive isolation jointly promoting speciation in the lake whitefish species complex (Coregonus clupeaformis). Journal of Evolutionary Biology 19: 1979–1994. http://dx.doi.org/10.1111/j.1420-9101.2006.01150.x

Romani S., Campuzano S., Macagno E.R. & Modolell J. 1989. Expression of achaete and scute genes in D. melanogaster imaginal discs and their function in sensory organ development. Genes & Development 3: 997–1007. http://dx.doi.org/10.1101/gad.3.7.997

Sander K. 1983. The evolution of patterning mechanisms: gleanings from insect embryogenesis and spermatogenesis. In: Goodwin B.C., Holder N. & Wylie C.C. (eds) Development and Evolution: 137–159. Cambridge University Press, Cambridge.

Scemama J.L., Hunter M., McCallam J., Prince V. & Stellwag E. 2002. Evolutionary divergence of vertebrate Hoxb2 expression patterns and transcriptional regulatory loci. Journal of Experimental Zoology (Molecular and Developmental Biology) 294: 285–299. http://dx.doi.org/10.1002/jez.90009

Schiff N.M., Feng Y., Quine J.A., Krasney P.A. & Cavener D.R. 1992. Evolution of the expression of the Gld gene in the reproductive tract of Drosophila. Molecular Biology and Evolution 9: 1029–1049.

Schlosser G. & Wagner G.P. 2003. Introduction: the modularity concept in developmental and evolutionary biology. In: Schlosser G. & Wagner G.P. (eds) Modularity in Development and Evolution: 1–11. University of Chicago Press, Chicago.

Scholtz G. 2008. Zoological detective stories: the case of the facetotectan crustacean life cycle. Journal of Biology 7: 16. http://dx.doi.org/10.1186/jbiol77

Schulmeister S. & Wheeler W.C. 2004. Comparative and phylogenetic analysis of developmental sequences. Evolution & Development 6: 50–57. http://dx.doi.org/10.1111/j.1525-142X.2004.04005.x

Siddall M.E. & Borda E. 2003. Phylogeny and revision of the leech genus Helobdella (Glossiphoniidae) based on mitochondrial gene sequences and morphological data and a special consideration of the triserialis complex. Zoologica Scripta 32: 23–33. http://dx.doi.org/10.1046/j.1463-6409.2003.00098.x

Skaer N., Pistillo D. & Simpson P. 2002. Transcriptional heterochrony of scute and changes in bristle pattern between two closely related species of blowfly. Developmental Biology 252: 31–45.

Slack J.M.W., Holland P.W.H. & Graham C.F. 1993. The zootype and the phylotypic stage. Nature 361: 490–492. http://dx.doi.org/10.1038/361490a0

Smith K.K. 1997. Comparative patterns of craniofacial development in eutherian and metatherian mammals. Evolution 51: 1663–1678. http://dx.doi.org/10.2307/2411218

Smith K.K. 2001. Heterochrony revisited: the evolution of developmental sequences. Biological Journal of the Linnean Society 73: 169–186. http://dx.doi.org/10.1111/j.1095-8312.2001.tb01355.x

Smith K.K. 2002. Sequence heterochrony and the evolution of development. Journal of Morphology 252: 82–97. http://dx.doi.org/10.1002/jmor.10014

Smith K.K. 2003. Time’s arrow: heterochrony and the evolution of development. International Journal of Developmental Biology 47: 613–621.

Song J.L., Wong J.L. & Wessel G.M. 2006. Oogenesis: single cell development and differentiation. Developmental Biology 300: 385–405. http://dx.doi.org/10.1016/j.ydbio.2006.07.041

Sørensen M.V., Funch P., Willerslev E., Hansen A.J. & Olesen J. 2000. On the phylogeny of the Metazoa in the light of Cycliophora and Micrognathozoa. Zoologischer Anzeiger 239: 297–318.

Southcott R.V. 1992. Revision of the larvae of Leptus Latreille (Acarina: Erythraeidae) of Europe and North America, with descriptions of post-larval instars. Zoological Journal of the Linnean Society 105: 1–153. http://dx.doi.org/10.1111/j.1096-3642.1992.tb01228.x

Stach T. 2014. Deuterostome phylogeny – a morphological perspective. In: Wägele J.W. & Bartolomaeus T. (eds) Deep Metazoan Phylogeny: The Backbone of the Tree of Life: 425–457. De Gruyter, Berlin.

Telford M.J. & Budd G.E. 2003. The place of phylogeny and cladistics in Evo-Devo research. International Journal of Developmental Biology 47: 479–490.

Theißen G. 2009. Saltational evolution: hopeful monsters are here to stay. Theory in Biosciences 128: 43–51. http://dx.doi.org/10.1007/s12064-009-0058-z

Thompson J.V. 1830. On the Cirripedes or Barnacles; demonstrating their deceptive character; the extraordinary Metamorphosis they undergo, and the Class of Animals to which they indisputably belong. In: Thompson J.V., Zoological Researches, and Illustrations; or, Natural History of Nondescript or Imperfectly Known Animals 1(1): 69–82. King and Ridings, Cork.

Thompson J.V. 1835. Discovery of the Metamorphosis in the Second Type of the Cirripedes, viz. the Lepades, Completing the Natural History of these singular Animals, and Confirming Their Affinity with the Crustacea. Philosophical Transactions of the Royal Society 126: 355–358. http://dx.doi.org/10.1098/rstl.1835.0022

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. http://dx.doi.org/10.1111/j.1525-142X.2011.00510.x

Tucker S.C. 1984. Origin of symmetry in flowers. In: White R.A. & Dickison W.C. (eds) Contemporary Problems in Plant Anatomy: 351–395. Academic Press, San Diego.

Velhagen W.A. Jr. 1997. Analyzing developmental sequences using sequence units. Systematic Biology 46: 204–210. http://dx.doi.org/10.1093/sysbio/46.1.204

von Baer K.E. 1828. Über Entwicklungsgeschichte der Thiere: Beobachtung und Reflexion 1. Bornträger, Königsberg.

Wagner G.P. 1989. The origin of morphological characters and the biological basis of homology. Evolution 43: 1157–1171. http://dx.doi.org/10.2307/2409354

Wagner G.P. 1996. Homologues, natural kinds and the evolution of modularity. American Zoologist 36: 36–43.

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. http://dx.doi.org/10.1038/nrg2949

Weisblat D.A. & Kuo D.-H. 2009. Helobdella (Leech): a model for developmental studies. In: Emerging Model Organisms – a Laboratory Manual 1: 245–267. CSHL Press, Cold Spring Harbor.

Werneburg I. & Sanchez-Villagra M.R. 2009. Timing of organogenesis support basal position of turtles in the amniote tree of life. BMC Evolutionary Biology 9: 82. http://dx.doi.org/10.1186/1471-2148-9-82

West-Eberhard M.J. 2003. Developmental Plasticity and Evolution. Oxford University Press, New York.

Wiens J.J. 2011. Re-evolution of lost mandibular teeth in frogs after more than 200 million years, and re-evaluating Dollo’s law. Evolution 65: 1283–1296. http://dx.doi.org/10.1111/j.1558-5646.2011.01221.x

Wiens J.J., Bonett R.M. & Chippindale P.T. 2005. Ontogeny discombobulates phylogeny: paedomorphosis and higher-level salamander relationships. Systematic Biology 54: 91–110. http://dx.doi.org/10.1080/10635150590906037

Wilson L.A.B., Schradin C., Mitgutsch C., Galliari F.C., Mess A. & Sánchez-Villagra M.R. 2010. Skeletogenesis and sequence heterochrony in rodent evolution, with particular emphasis on the African striped mouse, Rhabdomys pumilio (Mammalia). Organisms Diversity and Evolution 10: 243–258. http://dx.doi.org/10.1007/s13127-010-0020-4

Wray G.A., Hahn M.W., Abouheif E., Balhoff J.P., Pizer M., Rockman M.V. & Romano L.A. 2003. The evolution of transcriptional regulation in eukaryotes. Molecular Biology and Evolution 20: 1377–1419. http://dx.doi.org/10.1093/molbev/msg140

Wray G.A. & McClay D.R. 1989. Molecular heterochronies and heterotopies in early echinoid development. Evolution 43: 803–813. http://dx.doi.org/10.2307/2409308

Wülbeck C. & Simpson, P. 2000. Expression of achaete-scute homologues in discrete proneural clusters on the developing notum of the medfly C. capitata, suggests a common origin for the stereotyped bristle patterns of higher Diptera. Development 127: 1411–1420.

Wunderlin R.P. 1983. Revision of the arborescent Bauhinias (Fabaceae: Caesalpinioideae: Cercideae) native to middle America. Annals of the Missouri Botanical Garden 70: 95–127. http://dx.doi.org/10.2307/2399009

Yen S.H., Robinson G.S. & Quicke D.L.J. 2005. The phylogenetic relationships of Chalcosiinae (Lepidoptera, Zygaenoidea, Zygaenidae). Zoological Journal of the Linnean Society 143: 161–341. http://dx.doi.org/10.1111/j.1096-3642.2005.00139.x

Published
2015-06-08
How to Cite
Minelli, A. (2015). Biological Systematics in the Evo-Devo era. European Journal of Taxonomy, (125). https://doi.org/10.5852/ejt.2015.125