Home LiteratureArticle Details
PMID: 18522915 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Review

Review. Sympatric, parapatric or allopatric: the most important way to classify speciation?

Butlin RK, Galindo J, Grahame JW

Abstract

The most common classification of modes of speciation begins with the spatial context in which divergence occurs: sympatric, parapatric or allopatric. This classification is unsatisfactory because it divides a continuum into discrete categories, concentrating attention on the extremes, and it subordinates other dimensions on which speciation processes vary, such as the forces driving differentiation and the genetic basis of reproductive isolation. It also ignores the fact that speciation is a prolonged process that commonly has phases in different spatial contexts. We use the example of local adaptation and partial reproductive isolation in the intertidal gastropod Littorina saxatilis to illustrate the inadequacy of the spatial classification of speciation modes. Parallel divergence in shell form in response to similar environmental gradients in England, Spain and Sweden makes this an excellent model system. However, attempts to demonstrate 'incipient' and 'sympatric' speciation involve speculation about the future and the past. We suggest that it is more productive to study the current balance between local adaptation and gene flow, the interaction between components of reproductive isolation and the genetic basis of differentiation.

MeSH Terms
Adaptation, Biological/genetics Animal Structures/anatomy & histology Animals Demography Gene Flow/genetics Genetic Speciation Genetic Variation Genetics, Population Reproduction/genetics Snails/anatomy & histology,genetics Species Specificity
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Butlin Roger K
Department of Animal and Plant Sciences, University of Sheffield, Western Bank, Sheffield S10 2TN, UK. [email protected]
Galindo Juan
Grahame John W
References (42)
42 references, click to expand
  1. Relative contribution of dispersal and natural selection to the maintenance of a hybrid zone in Littorina.
    Evolution. 2004 Dec;58(12):2734-46 PMID: 15696751
  2. THE MAINTENANCE OF A CLINE IN THE MARINE SNAIL LITTORINA SAXATILIS: THE ROLE OF HOME SITE ADVANTAGE AND HYBRID FITNESS.
    Evolution. 1997 Dec;51(6):1838-1847 PMID: 28565125
  3. SYMPATRIC HOST RACE FORMATION AND SPECIATION IN FRUGIVOROUS FLIES OF THE GENUS RHAGOLETIS (DIPTERA, TEPHRITIDAE).
    Evolution. 1969 Jun;23(2):237-251 PMID: 28562891
  4. Nonallopatric and parallel origin of local reproductive barriers between two snail ecotypes.
    Mol Ecol. 2004 Nov;13(11):3415-24 PMID: 15488000
  5. Speciation by natural and sexual selection: models and experiments.
    Am Nat. 2002 Mar;159 Suppl 3:S22-35 PMID: 18707367
  6. Allopatric genetic origins for sympatric host-plant shifts and race formation in Rhagoletis.
    Proc Natl Acad Sci U S A. 2003 Sep 2;100(18):10314-9 PMID: 12928500
  7. Testing alternative models for sexual isolation in natural populations of Littorina saxatilis: indirect support for by-product ecological speciation?
    J Evol Biol. 2004 Mar;17(2):288-93 PMID: 15009262
  8. HYBRID ZONES WITH DOBZHANSKY-TYPE EPISTATIC SELECTION.
    Evolution. 1997 Aug;51(4):1027-1035 PMID: 28565489
  9. Evolution of adaptation through allometric shifts in a marine snail.
    Evolution. 2006 Dec;60(12):2490-7 PMID: 17263111
  10. The genetic architecture of ecological speciation and the association with signatures of selection in natural lake whitefish (Coregonus sp. Salmonidae) species pairs.
    Mol Biol Evol. 2007 Jun;24(6):1423-38 PMID: 17404398
  11. Natural selection at major histocompatibility complex loci of vertebrates.
    Annu Rev Genet. 1998;32:415-35 PMID: 9928486
  12. The power and promise of population genomics: from genotyping to genome typing.
    Nat Rev Genet. 2003 Dec;4(12):981-94 PMID: 14631358
  13. Review. The strength and genetic basis of reproductive isolating barriers in flowering plants.
    Philos Trans R Soc Lond B Biol Sci. 2008 Sep 27;363(1506):3009-21 PMID: 18579478
  14. Review. The genic view of plant speciation: recent progress and emerging questions.
    Philos Trans R Soc Lond B Biol Sci. 2008 Sep 27;363(1506):3023-36 PMID: 18579476
  15. Evidence for inversion polymorphism related to sympatric host race formation in the apple maggot fly, Rhagoletis pomonella.
    Genetics. 2003 Mar;163(3):939-53 PMID: 12663534
  16. Premating barriers to gene exchange and their implications for the structure of a mosaic hybrid zone between Chorthippus brunneus and C. jacobsi (Orthoptera: Acrididae).
    J Evol Biol. 2004 Jan;17(1):108-19 PMID: 15000654
  17. Phylogenetic evidence for multiple sympatric ecological diversification in a marine snail.
    Evolution. 2007 Jul;61(7):1600-12 PMID: 17598743
  18. REINFORCEMENT OF STICKLEBACK MATE PREFERENCES: SYMPATRY BREEDS CONTEMPT.
    Evolution. 1998 Feb;52(1):200-208 PMID: 28568163
  19. Selective maintenance of allozyme differences among sympatric host races of the apple maggot fly.
    Proc Natl Acad Sci U S A. 1997 Oct 14;94(21):11417-21 PMID: 11038585
  20. Site-specific genetic divergence in parallel hybrid zones suggests nonallopatric evolution of reproductive barriers.
    Mol Ecol. 2006 Nov;15(13):4021-31 PMID: 17054500
  21. Parallel speciation: a key to sympatric divergence.
    Trends Ecol Evol. 2001 Mar 1;16(3):148-153 PMID: 11179579
  22. Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits.
    Heredity (Edinb). 2008 Feb;100(2):158-70 PMID: 17314923
  23. Hybridization, ecological races and the nature of species: empirical evidence for the ease of speciation.
    Philos Trans R Soc Lond B Biol Sci. 2008 Sep 27;363(1506):2971-86 PMID: 18579473
  24. Speciation in reverse: morphological and genetic evidence of the collapse of a three-spined stickleback (Gasterosteus aculeatus) species pair.
    Mol Ecol. 2006 Feb;15(2):343-55 PMID: 16448405
  25. Natural selection and sympatric divergence in the apple maggot Rhagoletis pomonella.
    Nature. 2000 Oct 12;407(6805):739-42 PMID: 11048719
  26. MORPHOLOGICAL DIFFERENTIATION AND GENETIC COHESIVENESS OVER A MICROENVIRONMENTAL GRADIENT IN THE MARINE SNAIL LITTORINA SAXATILIS.
    Evolution. 1993 Dec;47(6):1770-1787 PMID: 28568008
  27. Review. Hybrid trait speciation and Heliconius butterflies.
    Philos Trans R Soc Lond B Biol Sci. 2008 Sep 27;363(1506):3047-54 PMID: 18579480
  28. The genetic basis for fruit odor discrimination in Rhagoletis flies and its significance for sympatric host shifts.
    Evolution. 2005 Sep;59(9):1953-64 PMID: 16261733
  29. Adaptation to a steep environmental gradient and an associated barrier to gene exchange in Littorina saxatilis.
    Evolution. 2006 Feb;60(2):268-78 PMID: 16610319
  30. Widespread parallel evolution in sticklebacks by repeated fixation of Ectodysplasin alleles.
    Science. 2005 Mar 25;307(5717):1928-33 PMID: 15790847
  31. Hawthorn-infesting populations of Rhagoletis pomonella in Mexico and speciation mode plurality.
    Evolution. 2007 May;61(5):1091-105 PMID: 17492964
  32. Sympatric speciation in Nicaraguan crater lake cichlid fish.
    Nature. 2006 Feb 9;439(7077):719-23 PMID: 16467837
  33. The way the world might be.
    J Evol Biol. 2005 Sep;18(5):1205-8 PMID: 16135115
  34. Geographic variation, speciation, and clines.
    Monogr Popul Biol. 1977;10:1-246 PMID: 409931
  35. Phenotypic plasticity in two marine snails: constraints superseding life history.
    J Evol Biol. 2006 Nov;19(6):1861-72 PMID: 17040383
  36. Postglacial intra-lacustrine divergence of Icelandic threespine stickleback morphs in three neovolcanic lakes.
    J Evol Biol. 2007 Sep;20(5):1870-81 PMID: 17714304
  37. "PATTERNS OF SPECIATION IN DROSOPHILA" REVISITED.
    Evolution. 1997 Feb;51(1):295-303 PMID: 28568795
  38. Islands increase genetic subdivision and disrupt patterns of connectivity of intertidal snails in a complex archipelago.
    Evolution. 2006 Dec;60(12):2498-506 PMID: 17263112
  39. Mate choice in divergent morphs of the gastropod mollusc Littorina saxatilis (Olivi): speciation in action?
    Anim Behav. 1999 Jul;58(1):181-184 PMID: 10413555
  40. Reproductive character displacement is not the only possible outcome of reinforcement.
    J Evol Biol. 2004 Jan;17(1):177-83 PMID: 15000660
  41. Sequence differentiation in regions identified by a genome scan for local adaptation.
    Mol Ecol. 2008 Jul;17(13):3123-35 PMID: 18510587
  42. Locus- and population-specific selection and differentiation between incipient species of Anopheles gambiae.
    Mol Biol Evol. 2007 Sep;24(9):2132-8 PMID: 17636041
Article Info
Journal
Philosophical transactions of the Royal Society of London. Series B, Biological sciences
Abbr.
Philos Trans R Soc Lond B Biol Sci
ISSN
1471-2970
Published
2008-09-27
Pages
2997-3007
Language
English
Region
England
NLM ID
7503623
PMCID
PMC2607313
Subset
IM
Grants
Biotechnology and Biological Sciences Research Council · United Kingdom
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]