Skip to main content
SpringerLink
Log in

Unpacking the species conundrum: philosophy, practice and a way forward

  • Review Article
  • Published:
Journal of Genetics Aims and scope Submit manuscript

Abstract

The history of ecology and evolutionary biology is rife with attempts to define and delimit species. However, there has been confusion between concepts and criteria, which has led to discussion, debate, and conflict, eventually leading to lack of consistency in delimitation. Here, we provide a broad review of species concepts, a clarification of category versus concept, an account of the general lineage concept (GLC), and finally a way forward for species discovery and delimitation. Historically, species were considered as varieties bound together by reproduction. After over 200 years of uncertainty, Mayr attempted to bring coherence to the definition of species through the biological species concept (BSC). This has, however, received much criticism, and the last half century has spawned at least 20 other concepts. A central philosophical problem is that concepts treat species as ‘individuals’ while the criteria for categorization treats them as ‘classes’. While not getting away from this problem entirely, the GLC attempts to provide a framework where lineage divergence is influenced by a number of different factors (and correlated to different traits) which relate to the different species concepts. We also introduce an ‘inclusive’ probabilistic approach for understanding and delimiting species. Finally, we provide a Wallacean (geography related) approach to the Linnaean problem of identifying and delimiting species, particularly for cases of allopatric divergence, and map this to the GLC. Going one step further, we take a morphometric terrain approach to visualizing and understanding differences between lineages. In summary, we argue that while generalized frameworks may work well for concepts of what species are, plurality and ‘inclusive’ probabilistic approaches may work best for delimitation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Ackermann R. R., Mackay A. and Arnold M. L. 2016 The hybrid origin of “modern” humans. Evol. Biol. 43, 1–11.

    Article  Google Scholar 

  • Avise J. C. and Johns G. C. 1999 Proposal for a standardized temporal scheme of biological classification for extant species. Proc. Natl. Acad. Sci. USA 96, 7358–7363.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baker A. J., Daugherty C. H., Colbourne R. and McLennan J. L. 1995 Flightless brown kiwis of New Zealand possess extremely subdivided population structure and cryptic species like small mammals. Proc. Natl. Acad. Sci. USA 92, 8254–8258.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boyd R. 1999 Homeostasis, species, and higher taxa. In Species: New Interdisciplinary Essays (ed. R. Wilson), pp. 141–185. MIT Press, Cambridge, USA.

    Google Scholar 

  • Chandrasekhara K., Kumar A. R. V. and Ganeshaiah K. N. 1998 Morphometric terrain as a technique to demarcate the species limits: a study using dung beetles. Project report submitted to Department of Science and Technology, GOI New Delhi, India.

  • Coyne J. A. and Orr H. A. 2004 Speciation. Sinauer Associates, Sunderland, USA.

    Google Scholar 

  • Cracraft J. L. 1983 Species concepts and speciation analysis. In Current Ornithology (ed. R. F. Johnston), pp. 159–187. Plenum Press, New York, USA.

    Chapter  Google Scholar 

  • Darwin C. 1859 On the Origin of Species by Means of Natural Selection, Or, the Preservation of Favoured Races in the Struggle for Life. J. Murray, London.

  • Darwin F. 1887 The life and letters of Charles Darwin, including an autobiographical chapter. John Murray, London, UK.

    Book  Google Scholar 

  • de Queiroz K. 1998 The General Lineage Concept of species, species criteria, and the process of speciation. In Endless forms: species and speciation (ed. D. J. Howard and S. H. Berlocher), pp. 57–75. Oxford University Press, Oxford, UK.

  • de Queiroz K. 2007 Species concepts and species delimitation. Syst. Biol. 56, 879–886.

    Article  PubMed  Google Scholar 

  • de Queiroz K. 2011 Branches in the lines of descent: Charles Darwin and the evolution of the species concept. Biol. J. Linn. Soc. 103, 19–35.

    Article  Google Scholar 

  • Dobzhansky T. 1937 Genetics and the origin of species. Columbia University Press, New York, USA.

    Google Scholar 

  • Dobzhansky T. 1950 Mendelian populations and their evolution. Am. Nat. 84, 401–418.

    Article  Google Scholar 

  • Donoghue M. J. 1985 A critique of the biological species concept and recommendations for a phylogenetic alternative. Bryologist Oct, 172–181.

  • Dover, G. 1995 A species definition: a functional approach. Trends Evol Evol 10, 489-490.

  • Dutton P. H., Davis S. K., Guerra T. and Owens D. 1996 Molecular phylogeny for marine turtles based on sequences of the ND4-leucine tRNA and control regions of mitochondrial DNA. Mol. Phylogenet. Evol. 5, 511–521.

    Article  CAS  PubMed  Google Scholar 

  • Eldredge N. and Cracraft J. L. 1980 Phylogenetic patterns and evolutionary process. Columbia University Press, New York, USA.

    Google Scholar 

  • Ereshefsky M. 1998 Species pluralism and anti-realism. Philosophy of Science 65, 103–120.

  • Ereshefsky M. 2007 Foundational issues concerning taxa and taxon names. Syst. Biol. 56, 295–301.

    Article  PubMed  Google Scholar 

  • Ereshefsky M. 2016 Species. In The Stanford encyclopedia of philosophy (summer 2016 edition) (ed. E. N. Zalta) (https://plato.stanford.edu/archives/sum2016/entries/species).

  • Fitzpatrick B. M. and Turelli M. 2006 The geography of mammalian speciation: mixed signals from phylogenies and range maps. Evolution 60, 601–615.

    Article  CAS  PubMed  Google Scholar 

  • Fouquet A., Vences M., Salducci M. D., Meyer A., Marty C., Blanc M. and Gilles A. 2007 Revealing cryptic diversity using molecular phylogenetics and phylogeography in frogs of the Scinax ruber and Rhinella margaritifera species groups. Mol. Phylogenet. Evol. 43, 567–582.

    Article  CAS  PubMed  Google Scholar 

  • Frey M. A. 2010 The relative importance of geography and ecology in species diversification: evidence from a tropical marine intertidal snail (Nerita). J. Biogeogr. 37, 1515–1528.

    Google Scholar 

  • Funk W. C., Angulo A., Caldwell J. P., Ryan M. J. and Cannatella D. C. 2008 Comparison of morphology and calls of two cryptic species of Physalaemus (Anura: Leiuperidae). Herpetologica 64, 290–304.

    Article  Google Scholar 

  • Ghiselin M. T. 1974 A radical solution to the species problem. Syst. Biol. 23, 536–544.

    Article  Google Scholar 

  • Gittleman J. L. and Pimm S. L. 1991 Crying wolf in North America. Nature 351, 524–525.

    Article  Google Scholar 

  • Grant P. R. and Grant B. R. 2015 Introgressive hybridization and natural selection in Darwin’s finches. Biol. J. Linn. Soc. 117, 812–822.

    Article  Google Scholar 

  • Hall J. P. W. 2005 Montane speciation patterns in Ithomiola butterflies (Lepidoptera: Riodinidae): are they consistently moving up in the world? Proc. R. Soc. London, Ser. B. 272, 2457–2466.

    Google Scholar 

  • Hamilton W. D. 1964 The genetical evolution of social behaviour. II. J. Theor. Biol. 7, 17–52.

    Article  CAS  PubMed  Google Scholar 

  • Hennig W. 1966 Phylogenetic systematics (ed. D. D. Davis and R. Zangerl) University of Illinois Press, Urbana-Champaign, USA.

  • Hull D. 1965 The effect of essentialism on taxonomy: two thousand years of stasis (I). Brit. J. Philos. Sci. 15, 314–326.

    Article  Google Scholar 

  • Hull D. 1978 A matter of individuality. Philos. Sci. 45, 335–360.

    Google Scholar 

  • Irwin D. E., Irwin J. H. and Price T. D. 2001 Ring species as bridges between microevolution and speciation. Genetica 112–113, 223–243.

    Article  PubMed  Google Scholar 

  • Jenks S. M. and Wayne R. K. 1992 Problems and policy for species threatened by hybridization: the red wolf as a case study. In Wildlife 2001: populations (ed. D. R. McCullough and R. H. Barrett), pp. 237–251. Springer Netherlands, New York, USA.

    Chapter  Google Scholar 

  • Joppa L. N., Roberts D. L., Myers N. and Pimm S. L. 2011 Biodiversity hotspots house most undiscovered plant species. Proc. Natl. Acad. Sci. USA 108, 13171–13176.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karl S. A. and Bowen B. W. 1999 Evolutionary significant units versus Geopolitical taxonomy: molecular systematics of and endangered sea turtle (Genus Chelonia). Conserv. Biol. 13, 990–999.

    Article  Google Scholar 

  • Karl S. A., Bowen B. W. and Avise J. C. 1995 Hybridization among the ancient mariners: characterization of marine turtle hybrids with molecular genetic assays. J. Hered. 86, 262–268.

    Article  CAS  PubMed  Google Scholar 

  • King M. 1993 Species evolution: the role of chromosome change. Cambridge University Press, Cambridge, USA.

    Google Scholar 

  • Kitcher P. 1984 Species. Philos. Sci. 51, 308–333.

    Article  Google Scholar 

  • Kumar V., Lammers F., Bidon T., Pfenninger M., Kolter L., Nilsson M. A. and Janke A. 2017 The evolutionary history of bears is characterized by gene flow across species. Sci. Rep. 7 (doi:10.1038/srep46487).

  • Linkem C. W., Hesed K. M., Diesmos A. C. and Brown R. M. 2010 Species boundaries and cryptic lineage diversity in a Philippine forest skink complex (Reptilia; Squamata; Scincidae: Lygosominae). Mol. Phylogenet. Evol. 56, 572–585.

    Article  PubMed  Google Scholar 

  • Mallet J. 2005 Hybridization as an invasion of the genome. Trends Evol Evol 20, 229–237.

  • Mallet J. 1995 A species definition for the modern synthesis. Trends Ecol. Evol. 10, 294–299.

    Article  CAS  PubMed  Google Scholar 

  • Mayden R. L. 1997 A hierarchy of species concepts: the denouement in the saga of the species problem. In Species: the units of diversity (ed. M. F. Claridge, H. A. Dawah and M. R. Wilson), pp. 381–423. Chapman and Hall, New York, USA.

    Google Scholar 

  • Mayr E. 1942 Systematics and the origin of species. Columbia University Press, New York, USA.

    Google Scholar 

  • Mayr E. 1963 Animal species and evolution. Harvard University Press, Massachusetts, USA.

    Book  Google Scholar 

  • Mayr E. and Ashlock P. D. 1991 Principles of systematic zoology, 2nd edition. McGraw-Hill, New York, USA.

  • Meier J. I., Marques D. A., Mwaiko S., Wagner C. E., Excoffier L. and Seehausen O. 2017 Ancient hybridization fuels rapid cichlid fish adaptive radiations. Nat. Commun. 8, 14363.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Michener C. D. 1970 Diverse approaches to systematics. Evol. Biol. 4, 1–38.

  • Millikan R. 1999 Historical kinds and the “special sciences”. Philos. Stud. 95, 45–65.

    Article  Google Scholar 

  • Mishler B. D. and Donoghue M.J. 1982 Species concepts: a case for pluralism. Syst. Zool. 31, 491–503.

  • Mishler B. D. 1985 The morphological, developmental, and phylogenetic basis of species concepts in bryophytes. Bryologist Oct, 207–14.

  • Myers N., Mittermeier R. A., Mittermeier C. G., da Fonseca G. A. and Kent J. 2000 Biodiversity hotspots for conservation priorities. Nature 403, 853–858.

    Article  CAS  PubMed  Google Scholar 

  • Nelson G. J. and Platnick N. I. 1981 Systematics and biogeography: cladistics and vicariance. Columbia University Press, New York, USA.

    Google Scholar 

  • Nixon K. C. and Wheeler Q. D. 1990 An amplification of the phylogenetic species concept. Cladistics 6, 211–223.

    Article  Google Scholar 

  • Nowak R. 1995 Hybridization: the double-edged threat. Canid News 3, 2–6.

    Google Scholar 

  • Paterson H. E. H. 1985 The recognition concept of species. In Species and speciation (ed. E. S. Vrba), pp. 21–29. Transvaal Museum, Pretoria, South Africa.

    Google Scholar 

  • Phillimore A. B., Orme C. D. L., Thomas G. H., Blackburn T. M., Bennett P. M., Gaston K. J. and Owens I. P. F. 2008 Sympatric speciation in birds is rare: Insights from range data and simulations. Am. Nat. 171, 646–657.

    Article  PubMed  Google Scholar 

  • Reydon T. A. C. 2005 On the nature of the species problem and the four meanings of ‘species’. Stud. Hist. Philos. Biol. Biomed. Sci. 36, 135–158.

    Article  PubMed  Google Scholar 

  • Ridley M. 1993 Evolution. Blackwell Scientific, Boston, USA.

    Google Scholar 

  • Rosen D. E. 1979 Fishes from the uplands and intermontane basins of Guatemala: revisionary studies and comparative biogeography. Bull. Am. Mus. Nat. Hist. 162, 267–376.

    Google Scholar 

  • Shanker K. 2001 A review of species concepts: ideas for a new concept and implications for the green–black turtle debate. Twenty first Annual Symposium on Sea Turtle Biology and Conservation. Philadelphia, USA.

  • Simpson G. G. 1951 The species concept. Evolution 5, 285–298.

  • Simpson G. G. 1961 Principles of animal taxonomy. Columbia University Press, New York, USA.

  • Sokal R. R. and Sneath P. H. A. 1963 Principles of numerical taxonomy. Freeman, San Francisco, USA.

  • Sokal R. R. and Crovello T. J. 1970 The biological species concept: a critical evaluation. Am. Nat. 104, 127–153.

    Article  Google Scholar 

  • Soubrier J., Gower G., Chen K., Richards S. M., Llamas B., Mitchell K. J. et al. 2016 Early cave art and ancient DNA record the origin of European bison. Nat. Commun. 7 (doi:10.1038/ncomms13158).

  • Templeton A. R. 1989 The meaning of species and speciation: a genetic perspective. In: Speciation and its Consequences (eds D. Otte and J. A. Endler), pp. 3–27. Sinauer, Sunderland, USA.

  • Van Valen L. 1976 Ecological species, multispecies, and oaks. Taxon 25, 233–239.

    Article  Google Scholar 

  • Vences M., Thomas M., Bonett R. M. and Vieites D. R. 2005 Deciphering amphibian diversity through DNA barcoding: chances and challenges. Philos. Trans. R. Soc. London, Ser. B 360, 1859–1868.

    Article  CAS  Google Scholar 

  • Vijayakumar S. P., Dinesh K. P., Prabhu M. V. and Shanker K. 2014 Lineage delimitation and description of nine new species of bush frogs (Anura: Raorchestes, Rhacophoridae) from the Western Ghats Escarpment. Zootaxa 3893, 451–488.

    Article  CAS  PubMed  Google Scholar 

  • Vijayakumar S. P., Menezes R. C., Jayarajan A. and Shanker K. 2016 Glaciations, gradients, and geography: multiple drivers of diversification of bush frogs in the Western Ghats Escarpment. Proc. R. Soc. London, Ser. B 283, 20161011.

    Article  Google Scholar 

  • Wallace A. R. 1865 On the phenomena of variation and geographical distribution as illustrated by the Papilionidae of the Malayan region. Trans. Linn. Soc. Lond. 25, 1–71.

    Article  Google Scholar 

  • Whittaker R. J., Araújo M. B., Paul J., Ladle R. J., Watson J. E. and Willis K. J. 2005 Conservation biogeography: assessment and prospect. Divers. Distrib. 11, 3–23.

    Article  Google Scholar 

  • Wiens J. J. and Graham C. H. 2005 Niche conservatism: integrating evolution, ecology, and conservation biology. Annu. Rev. Ecol. Evol. Syst. 36, 519–539.

    Article  Google Scholar 

  • Wiens J. J. and Penkrot T. A. 2002 Delimiting species using DNA and morphological variation and discordant species limits in spiny lizards (Sceloporus). Syst. Biol. 51, 69–91.

    Article  PubMed  Google Scholar 

  • Wiley E. O. 1978 The evolutionary species concept reconsidered. Syst. Zool. 27, 17–26.

    Article  Google Scholar 

  • Wilkins J. S. 2006a Species, kinds, and evolution. Rep. Cent. Natl. Sci. Edu. 26, 36–45.

    Google Scholar 

  • Wilkins J. S. 2006b A list of 26 species ‘concepts’. Sci. Blogs (http://scienceblogs.com/evolvingthoughts/2006/10/01/a-list-of-26-species-concepts/, accessed 5 January 2017).

  • Wilkins J. S. 2009 Species: a history of the idea. University of California Press, Berkeley, USA.

  • Wilson E. O. 1992 The diversity of life. Penguin Books, London.

  • Wilson R. 1999 Realism, essence, and kind: resuscitating species essentialism? In Species: new interdisciplinary studies (ed. R. Wilson). MIT Press Cambridge, Cambridge, USA.

    Google Scholar 

  • Wilson P. J., Grewal S. K., Mallory F. F. and White B. N. 2009 Genetic characterization of hybrid wolves across Ontario. J. Hered. 100, 80–89.

    Article  Google Scholar 

  • Young D. 2007 The discovery of evolution. Cambridge University Press, Cambridge, UK.

    Google Scholar 

  • Zachos F. E. 2016 Species Concepts in Biology: Historical Development, Theoretical Foundations and Practical Relevance. Springer.

Download references

Acknowledgements

The authors, like most other evolutionary biologists around the world, have been pondering the species question throughout their respective careers. KS started his musings in a not-so-quiet corner of the Wildlife Institute of India, aided by spirited conversations with Jagdish Krishnaswamy, M. S. Chaitra and Meera Anna Oommen, and inspired by a ‘scruffy dog’ that became a symbol of the ‘good’ vs ‘bad’ species conundrum. SPV got embroiled in it when he joined KS’s lab as a graduate student and became obsessed with questions regarding the origin and diversification of bush frogs and other herpetofauna in the Western Ghats. KNG has got into the habit of attempting to solve intractable problems over several decades, abetted by his colleagues R. Uma Shaanker and K. Chandrashekara. We would like to thank all the reviewers and editors for their constructive comments on the manuscript.

Author information

Authors and Affiliations

  1. Centre for Ecological Sciences, Indian Institute of Science, Bengaluru,  560 012, India

    Kartik Shanker & S. P. Vijayakumar

  2. A-001, Samvriddhi Gardenia Apartments, 88/3, Byataranapura, Near Sahakara Nagar A Block, Bengaluru,  560 092, India

    Kartik Shanker

  3. Royal Enclave, Srirampura, Jakkur Post, Bengaluru,  560 064, India

    Kartik Shanker & K. N. Ganeshaiah

  4. School of Ecology and Conservation, University of Agricultural Sciences, GKVK, Bengaluru,  560 065, India

    K. N. Ganeshaiah

Authors
  1. Kartik Shanker
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. P. Vijayakumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. K. N. Ganeshaiah
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kartik Shanker.

Additional information

Corresponding editor: T. N. C. Vidya

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shanker, K., Vijayakumar, S.P. & Ganeshaiah, K.N. Unpacking the species conundrum: philosophy, practice and a way forward. J Genet 96, 413–430 (2017). https://doi.org/10.1007/s12041-017-0800-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12041-017-0800-0

Keywords

Search

Navigation