Title: So what is a species anyway? A primatological perspective
Abstract: Evolutionary Anthropology: Issues, News, and ReviewsVolume 23, Issue 1 p. 21-23 IssuesOpen Access So what is a species anyway? A primatological perspective Dietmar Zinner, Dietmar ZinnerSearch for more papers by this authorChristian Roos, Christian RoosSearch for more papers by this author Dietmar Zinner, Dietmar ZinnerSearch for more papers by this authorChristian Roos, Christian RoosSearch for more papers by this author First published: 20 February 2014 https://doi.org/10.1002/evan.21390Citations: 7 Corresponding author: Christian Roos: phone +49–551-3851-300, fax +49–551-3851-372, e-mail [email protected] Dietmar Zinner is senior scientist in the Cognitive Ethology Laboratory of the German Primate Center and lecturer at the University of Göttingen, Germany. He has worked on the behavior, ecology and phylogeography of baboons and Malagasy lemurs. His main research interests are the evolution of primate social systems, primate phylogeography. and primate ecology. E-mail: [email protected] Christian Roos is a senior scientist at the German Primate Center and lecturer at the University of Göttingen. He is head of the Gene Bank of Primates and Vice Chair of the Southeast Asian/Indochinese section of the IUCN/SSC Primate Specialist Group. His main research interests are the evolution and phylogeography of primates. E-mail: [email protected] AboutSectionsPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinked InRedditWechat Abstract Since Darwin's time, the question "what a species" has provoked fierce disputes and a tremendous number of publications, from short opinion papers to thick volumes.1 The debates covered fundamental philosophical questions, such as: Do species exist at all independently of a human observer or are they just a construct of the human mind to categorize nature's organismic diversity and serve as a semantic tool in human communication about biodiversity?2-4 or: Are species natural kinds (classes) or individuals that are "born" by speciation, change in course of time, and finally "die" when they go extinct or diverge into new species?5-8 Also included was the problem of species as taxa (taxonomic) versus species as products of the speciation process (evolutionary).9 More pragmatic issues arose, such as: How can we reliably delineate and delimitate species?10, 11 The great interest in what a species is reflects the importance of "species" as fundamental units in most fields of biology, especially evolutionary biology, ecology, and conservation.2, 12-14 More than twenty species concepts have been proposed to answer the question of what a species is. However, a generally accepted concept is not available.15 In principle, we are still at the same point that Darwin was 1859, when he wrote: "No one definition has satisfied all naturalists; yet every naturalist knows vaguely what he means when he speaks of a species."16:44 Given that biologists have spent decades trying to find a universal definition of "species" and have not achieved it, it has become obvious that there is no single correct definition. As an alternative, a pluralistic, approach was proposed, where different species concepts are equally legitimate and useful in classifying organisms and understanding the history of life, although many people find this unsatisfying.17-19 Another question is whether species, particularly as a taxonomic rank, means the same in different groups, such as prokaryotes, plants, invertebrates, and mammals.20, 21 For instance, we have to ask whether a macaque species and a baboon species are really the same rank, given that most macaque species constitute phylogenetically much older lineages than do baboon species, and thus are genetically more heterogeneous.22 In primatology, the number of species has increased tremendously within recent years. Rowe,23 in 1996, listed 230 species; Groves,24 in 2001, listed >350 species; and in the third volume of the Handbook of the Mammals of the World,25 published in 2013, the number of species exceeds 480. This increase is partly a result of discoveries of formerly unknown primates in the wild, among them Rungwecebus kipunji26 and Rhinopithecus strykeri27 or Cercopithecus lomamiensis,28 but it is more strongly a consequence of the use of molecular methods in phylogenetic studies and the use of differences in DNA sequences to delimit species. This, combined with the application of a Phylogenetic Species Concept31 has caused the increase in species numbers in primates as in most other studied taxonomic groups, such as birds32 or bovids.33 This led Ian Tattersall34 to pose the question, "Madagascar's lemurs: cryptic diversity or taxonomic inflation?" This question can be generalized for all primate and nonprimate lineages.35 The increase in species, the splitting of genera, and the constantly changing primate species list have recently created uncertainty about primate taxonomy and fueled a controversy about the usefulness of particular species concepts and the criteria that should be applied to delineate and delimit species.36-42 In our previous work, we have contributed to this species increase (e.g. 43-48) by applying an integrative approach49 using information from mitochondrial DNA, chromosomes, morphology, behavior, acoustics, and biogeography to delimit new taxa. Based on this information, the identification of phylogenetic clades or evolutionary units was relatively easy, and conservatively, we ranked the detected biological entities or clades as subspecies or species. We did this with hesitation because whether such units should be given species rank in a Linnean classification was a question we were, in fact, unable to decide. The increase in species, the splitting of genera, and the constantly changing primate species list have recently created uncertainty about primate taxonomy and fueled a controversy about the usefulness of particular species concepts and the criteria that should be applied to delineate and delimit species.36-42 Here, our aim is not to provide a solution to the species problem or present another "new species concept" because we think that a general species concept, according to which species are classes in a classification scheme (sensu Linné) and not biological entities is an unattainable solution. We see a species as a group of individuals that are vertically connected by descent and/or horizontally by sexual gene exchange.50-52 Our main problem is not identifying or distinguishing such entities, but whether it is justified to give them a rank (genus, species, subspecies) in the classification scheme.53 For us, it also remains questionable whether giving a species, as a product of speciation, a rank at all. We also wonder whether the Linnean hierarchical taxonomy should be abandoned and a rank-independent nomenclature used instead (for example, "species" in a non-Linnean sense, "taxon," or "evolutionary significant unit"). We see a biological species as a group of individuals that are vertically connected by descent and/or horizontally by sexual gene exchange. Our main problem is not identifying or distinguishing such entities, but whether it is justified to give them a rank (genus, species, subspecies) in the classification scheme. When delimitating "species," we face two challenges: how to identify phylogenetic clusters, groups, or evolutionary entities when regarding species as products of the speciation process (vertical gene flow) and how to determine the degree of horizontal gene flow among such entities, given that pre- and postzygotic barriers are not complete and occasional sexual contacts occur between entities. The first challenge can be addressed by applying cladistic methods54 to either molecular or other characters to define exclusive (monophyletic) entities. The second challenge is more difficult. In many cases, genealogical discordances caused by both historical and ongoing gene flow between entities are detectable with molecular methods.55-57 This makes delimitation of exclusive entities based on only one or a few genetic markers questionable.39-58 An extreme example is the case of Rungwecebus kipunji. If this species had been delimitated just on the basis of mitochondrial sequence information, the introgressed population in the Southern Highlands of Tanzania, would have been classified as a baboon and the second, the nonintrogressed population at Ndundulu, Tanzania carrying the original Rungwecebus mitochondria, would have been delineated as Rungwecebus.59-61 To obtain an estimate of gene flow between closely related species, such as in brown lemurs or tarsiers, population genetic approaches are indicated.62, 63 In such analyses, it often becomes obvious that a certain degree of gene flow occurs. Most importantly, some genes might be affected whereas others might not.64 Interestingly, occasional horizontal exchange of genes does not, per se, break the exclusivity or identity of species. It might become more important to identify particular genes that hinder complete fusion of entities or genes that cause reproductive incompatibilities.65 An approach that will become increasingly applicable as genetic data on nonmodel organisms accumulates is a multi-locus coalescent-based method that specifically links patterns of lineage divergence to speciation and demographic processes.64, 66, 67 Such large population genomic datasets have the potential to investigate the role of gene exchange in the speciation process. An approach that will become increasingly applicable as genetic data on nonmodel organisms accumulates is a multi-locus coalescent-based method that specifically links patterns of lineage divergence to speciation and demographic processes. Our approach is based on a Phylogenetic Species Concept,68 but adds, if possible, information on horizontal gene flow, which is part of the Biological Species Concept.69 However, we think, as explained earlier, that the Linnean system is not suitable for the classification of species, although, its nomenclature is still important for practical reasons. Without question, a universal taxonomic communication system is needed. REFERENCES 1 Wilkins JS. 2009. Species: a history of the idea. Berkeley: California University Press. CrossrefGoogle Scholar 2 Mayr E. 1996. What is a species and what is not? Philos Sci 63: 262– 277. CrossrefWeb of Science®Google Scholar 3 Stamos DN. 2003. The species problem: biological species, ontology, and the metaphysics of biology. Lanham: Lexington Books. Google Scholar 4 Willmann R. 2010. Darwins Artbegriff und heutige Artkonzepte in der Zoologie. Braunschweiger naturkundliche Schriften 9: 95– 134. Google Scholar 5 Ghiselin MT. 1974. A radical solution to the species problem. Syst Zool 23: 536– 544. CrossrefWeb of Science®Google Scholar 6 Hull DL. 1976. Are species really individuals? Syst Zool 25: 174– 191. CrossrefWeb of Science®Google Scholar 7 Reydon TAC. 2009. Species and kinds: a critique of Rieppel's ''one of a kind'' account of species. Cladistics 25: 1– 8. Wiley Online LibraryWeb of Science®Google Scholar 8 Kunz W. 2012. Do species exist? Principles of taxonomic classification. Weinheim: Wiley– VCH. Google Scholar 9 Endler JA. 1989. Conceptual and other problems in speciation. In: D Otte, JA Endler, editors. Speciation and its consequences. Sunderland: Sinauer Associates. p 625– 648. Google Scholar 10 Claridge MF, Dawah HA, Wilson MR. 1997. Practical approaches to species concepts for living organisms. In: MF Claridge, HA Dawah, MR Wilson, editors. Species: the units of biodiversity. London: Chapman & Hall. p 1– 15. Google Scholar 11 Groves CP. 2012. Species concept in primates. Am J Primatol 74: 687– 691. Wiley Online LibraryPubMedWeb of Science®Google Scholar 12 Mace GM. 2004. The role of taxonomy in species conservation. Philos Trans R Soc Lond B 359: 711– 719. CrossrefPubMedWeb of Science®Google Scholar 13 MacLaurin J, Sterelny K. 2008. What is biodiversity? Chicago: The University of Chicago Press. CrossrefGoogle Scholar 14 Frankham R, Ballou JD, Dudash MR, et al. 2012. Implications of different species concepts for conserving biodiversity. Biol Conserv 153: 25– 31. CrossrefWeb of Science®Google Scholar 15 Wilkins JS. 2009. Defining species: a sourcebook from antiquity to today. New York: Peter Lang. Google Scholar 16 Darwin C. 1859. On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. London: Murray. CrossrefGoogle Scholar 17 Dupré J. 1999. On the impossibility of a monistic account of species. In: RA Wilson, editor. Species: new interdisciplinary essays. London: MIT Press. p 3– 22. Web of Science®Google Scholar 18 Ereshefsky M. 1992. Eliminative pluralism. Philos Sci 59: 671– 690. CrossrefWeb of Science®Google Scholar 19 Mishler BD, Donoghue MJ. 1982. Species concepts: a case for pluralism. Syst Zool 31: 491– 503. CrossrefWeb of Science®Google Scholar 20 Avise JC, Liu JX. 2011. On the temporal inconsistencies of Linnean taxonomic ranks. Biol J Linnean Soc 102: 707– 714. Wiley Online LibraryWeb of Science®Google Scholar 21 Vences M, Guayasamin JM, Miralles A, et al. 2013. To name or not to name: criteria to promote economy of change in Linnaean classification schemes. Zootaxa 3636: 201– 244. CrossrefPubMedWeb of Science®Google Scholar 22 Finstermeier K, Zinner D, Brameier M, et al. 2013. A mitogenomic phylogeny of living primates. PLoS ONE 8: e69504. CrossrefCASPubMedWeb of Science®Google Scholar 23 Rowe N. 1996. The pictorial guide to the living primates. East Hampton: Pogonias Press. Google Scholar 24 Groves CP. 2001. Primate taxonomy. Washington DC: Smithsonian Institution Press. Google Scholar 25 Mittermeier RA, Rylands AB, Wilson DE. 2013. The handbook of the mammals of the world, vol. 3. Primates. Barcelona: Lynx Edicions. Google Scholar 26 Jones T, Ehardt CL, Butynski TM, et al. 2005. The highland mangabey Lophocebus kipunji: a new species of African monkey. Science 308: 1161– 1164. CrossrefCASPubMedWeb of Science®Google Scholar 27 Geissmann T, Lwin N, Aung SS, et al. 2010. A new species of snub-nosed monkey, genus Rhinopithecus Milne-Edwards, 1872 (Primates, Colobinae), from northern Kachin state, northeastern Myanmar. Am J Primatol 73: 96– 107. Wiley Online LibraryWeb of Science®Google Scholar 28Hart JA, Detwiler KM, Gilbert CC, et al. 2012. Leusula: A new species of Cercopithecus monkey endemic to the Democratic Republic of Congo and implications for conservation of Congo's Central Basin. PLoS ONE 7: e44271. CrossrefCASPubMedWeb of Science®Google Scholar 29 Blaxter ML. 2004. The promise of a DNA taxonomy. Philos Trans R Soc B 359: 669– 679. CrossrefCASPubMedGoogle Scholar 30 Meier R. 2008. DNA sequences in taxonomy: opportunities and challenges. In: QD Wheeler, editor. The new taxonomy. Boca Raton: CRC Press. p 95– 128. CrossrefGoogle Scholar 31 Cracraft J. 1983. Species concepts and speciation analysis. In: RF Johnston, DM Power, editors. Current ornithology. New York: Plenum Press. p 159– 187. CrossrefGoogle Scholar 32 Dillon S, Fjeldså J. 2005. The implications of different species concepts for describing biodiversity patterns and assessing conservation needs for African birds. Ecography 28: 682– 692. Wiley Online LibraryWeb of Science®Google Scholar 33 Heller R, Frandsen P, Lorenzen ED, et al. 2013. Are there really twice as many bovid species as we thought? Syst Biol 62: 490– 493. CrossrefPubMedWeb of Science®Google Scholar 34 Tattersall I. 2007. Madagascar's lemurs: cryptic diversity or taxonomic inflation? Evol Anthropol 16: 12– 23. Wiley Online LibraryWeb of Science®Google Scholar 35 Isaac NJB, Mallet J, Mace GM. 2004. Taxonomic inflation: its influence on macroecology and conservation. Trends Ecol Evol 9: 464– 469. CrossrefWeb of Science®Google Scholar 36 Gippoliti S, Groves CP. 2012. "Taxonomic inflation" in the historical context of mammalogy and conservation. Hystrix, Ital J Mammal 23: 8– 11. Web of Science®Google Scholar 37 Gippoliti S, Cotterill FPD, Groves CP. n. d. Mammal taxonomy without taxonomists: a reply to Zachos and Lovari. Hystrix, Ital J Mammal 24. In press. Google Scholar 38 Groves CP. 2013. The nature of species: a rejoinder to Zachos et al. Mammalian Biol 78: 7– 9. CrossrefWeb of Science®Google Scholar 39 Markolf M, Brameier M, Kappeler P. 2011. On species delimitation: yet another lemur species or just genetic variation? BMC Evol Biol 11: 216. CrossrefPubMedWeb of Science®Google Scholar 40 Zachos FE, Apollonio M, Bärmann EV, et al. 2013. Species inflation and taxonomic artefacts: a critical comment on recent trends in mammalian classification. Mamm Biol 78: 1– 6. CrossrefWeb of Science®Google Scholar 41 Zachos FE, Clutton-Brock T, Festa-Bianchet M, et al. 2013. Taxonomy: species splitting puts conservation at risk. Nature 494: 35– 35. CrossrefCASPubMedWeb of Science®Google Scholar 42 Zachos FE, Lovari S. n. d. Taxonomic inflation and the poverty of the phylogenetic species concept: a reply to Gippoliti and Groves. Hystrix, Ital J Mammal 24. In press. Google Scholar 43 Kappeler PM, Rasoloarison RM, Razafimanantsoa L, et al. 2005. Morphology, behaviour and molecular evolution of giant mouse lemurs (Mirza spp.) Gray, 1870, with description of a new species. Primate Rep 71: 3– 26. Google Scholar 44 Andriaholinirina N, Fausser JL, Roos C, et al. 2006. Molecular phylogeny and taxonomic revision of the sportive lemurs (Lepilemur, Primates). BMC Evol Biol 6: 17. CrossrefCASPubMedWeb of Science®Google Scholar 45 Rabarivola C, Zaramody A, Fausser JL, et al. 2006. Cytogenetic and molecular characteristics of a new species of sportive lemur from Northern Madagascar. Lemur News 11: 45– 49. Google Scholar 46 Zaramody A, Fausser JL, Ross C, et al. 2006. Molecular phylogeny and taxonomic revision of the eastern woolly lemurs (Avahi laniger). Primate Rep 74: 9– 23. Google Scholar 47 Roos C, Nadler T, Walter L. 2008. Mitochondrial phylogeny, taxonomy and biogeography of the silvered langur species group (Trachypithecus cristatus). Mol Phylogenet Evol 47: 629– 636. CrossrefCASPubMedWeb of Science®Google Scholar 48 Thinh VN, Mootnick AR, Thanh VN, et al. 2010. A new species of crested gibbon, from the central Annamite mountain range. Vietnamese J Primatol 1: 1– 12. Google Scholar 49 Schlick-Steiner BC, Steiner FM, Seifert B, et al. 2009. Integrative taxonomy: a multisource approach to exploring biodiversity. Ann Rev Entomol 55: 421– 438. CrossrefCASWeb of Science®Google Scholar 50de Queiroz K, Donoghue MJ. 1988. Phylogenetic systematics and the species problem. Cladistics 4: 317– 338. Wiley Online LibraryWeb of Science®Google Scholar 51de Queiroz K. 1998. The general lineage concept of species, species criteria, and the process of speciation. A conceptual unification and terminological recommendations. In: DJ Howard, SH Berlocher, editors. Endless Forms: Species and Speciation New York: Oxford University Press. p 57– 75. Google Scholar 52de Queiroz K. 2007. Species concepts and species delimitation. Syst Biol 56: 879– 886. CrossrefPubMedWeb of Science®Google Scholar 53 Baum DA. 2009. Species as ranked taxa. Syst Biol 58: 74– 86. CrossrefPubMedWeb of Science®Google Scholar 54 Hennig W. 1966. Phylogenetic systematics. Urbana: Illinois University Press. PubMedWeb of Science®Google Scholar 55 Arnold ML, Meyer A. 2006. Natural hybridization in primates: one evolutionary mechanism. Zoology 109: 261– 276. CrossrefPubMedWeb of Science®Google Scholar 56 Roos C, Zinner D, Kubatko L, et al. 2011. Nuclear versus mitochondrial DNA: evidence for hybridization in colobine monkeys. BMC Evol Biol 11: 77. CrossrefPubMedWeb of Science®Google Scholar 57 Zinner D, Arnold ML, Roos C. 2011. The strange blood: natural hybridization in primates. Evol Anthropol 20: 96– 103. Wiley Online LibraryPubMedWeb of Science®Google Scholar 58 Nichols R. 2001. Gene trees and species trees are not the same. Trends Ecol Evol 16: 358– 364. CrossrefCASPubMedWeb of Science®Google Scholar 59 Burrell AS, Jolly CJ, Tosi AJ, et al. 2009. Mitochondrial evidence for the hybrid origin of the kipunji, Rungwecebus kipunji (Primates: Papionini). Mol Phylogenet Evol 51: 340– 348. CrossrefCASPubMedWeb of Science®Google Scholar 60 Roberts TE, Davenport TRB, Hildebrandt KBP, et al. 2010. The biogeography of introgression in the critically endangered African monkey Rungwecebus kipunji. Biol Lett 6: 233– 237. CrossrefPubMedWeb of Science®Google Scholar 61 Zinner D, Arnold ML, Roos C. 2009. Is the new primate genus Rungwecebus a baboon? PLoS ONE 4: e4859. CrossrefCASPubMedWeb of Science®Google Scholar 62 Pastorini J, Zaramody A, Curtis D, et al. 2009. Genetic analysis of hybridization and introgression between wild mongoose and brown lemurs. BMC Evol Biol 9: 32. CrossrefCASPubMedWeb of Science®Google Scholar 63 Merker S, Driller C, Perwitasari-Farajallah D, et al. 2009. Elucidating geological and biological processes underlying the diversification of Sulawesi tarsiers. Proc Natl Acad Sci USA 106: 8459– 8464. CrossrefCASPubMedWeb of Science®Google Scholar 64 Tung J, Alberts SC, Wray GA 2010. Evolutionary genetics in wild primates: combining genetic approaches with field studies of natural populations. Trends Genet 26: 353– 362. CrossrefCASPubMedWeb of Science®Google Scholar 65 Abbott R, Albach D, Ansell S, et al. 2013. Hybridization and speciation. J Evol Biol 26: 229– 246. Wiley Online LibraryCASPubMedWeb of Science®Google Scholar 66 Bryant D, Bouckaert R, Felsenstein J, et al. 2012. Inferring species trees directly from biallelic genetic markers: bypassing gene trees in a full coalescent analysis. Mol Biol Evol 29: 1917– 1932. CrossrefCASPubMedWeb of Science®Google Scholar 67 Fujita MK, Leaché AD, Burbrink FT, et al. 2012. Coalescent-based species delimitation in an integrative taxonomy. Trends Ecol Evol 27: 480– 488. CrossrefPubMedWeb of Science®Google Scholar 68 Eldredge N, Cracraft J. 1980. Phylogenetic patterns and the evolutionary process: method and theory in comparative biology. New York: Columbia University Press. Google Scholar 69 Mayr E. 1942. Systematics and the origin of species from the viewpoint of a zoologist. New York: Columbia University Press. Google Scholar Citing Literature Volume23, Issue1January/February 2014Pages 21-23 ReferencesRelatedInformation