Abstract
After decades of debates about species concepts, there is broad agreement that species are evolving lineages. However, species classification is still in a state of disorder: different methods of delimitation lead to competing outcomes for the same organisms, and the groups recognised as species are of widely different kinds. This paper considers whether this problem can be resolved by developing a unitary scale for evolutionary independence. Such a scale would show clearly when groups are comparable and allow taxonomists to choose a conventional threshold of independence for species status. Existing measurement approaches to species delimitation are typically shot down by what I call the heterogeneity objection, according to which independently evolving groups are too heterogeneous to be captured by a single scale. I draw a parallel with the measurement of temperature to argue that this objection does not provide sufficient reasons to abandon the measurement approach, and that such an approach may even help to make the vague notion of evolutionary independence more precise.
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Notes
Note that by this continuum I do not mean a sequence of different indicators of evolutionary independence (e.g. diagnosability, reproductive isolation, etc.) such as on De Queiroz’ famous diagram of diverging lineages (De Queiroz 1998, p. 64, Fig. 5.4). De Queiroz’ diagram is problematic because these indicators often occur in different orders, shapes, and combinations. Instead, I propose thinking of evolutionary independence as a quantity (perhaps ordinal) that any group of populations has to some degree.
The connection between species delimitation and measurement has been made in philosophy too. More precisely, Conix (2018) draws an analogy between measurement and integrative methods of species delimitation. The claim in this paper is more radical, however, as I do not merely draw an analogy between one taxonomic method and measurement in the physical sciences, but instead propose to see species delimitation as a form of measurement.
It is typically referred to as the Tobias criteria, referring to the multiple parameters in the model. I use ‘criterion’ here to emphasize that it integrates these parameters into a single score for species status.
Indeed, it could be argued that a viable measurement approach should build on existing measures such as those of genetic divergence, population connectivity and the strength of isolation barriers (Coyne and Orr 1989; Palsbøll et al. 2007; Lowe and Allendorf 2010; Sobel et al. 2010). However, the Tobias criterion takes none of these into account.
For another apt example, see Chang’s (2004, chapter 2) discussion of how Regnault showed the air thermometer to be more reliable than the mercury thermometer without making substantial theoretical commitments.
References
Alexandrova A, Haybron D (2016) Is construct validation valid? Philos Sci 83:1089–1109
Bacon F (1902) Novum Organum. P.F. Collier, New York
Balen S, Eaton JA, Rheindt FE (2013) Biology, taxonomy and conservation status of the short-tailed Green Magpie Cissa [t.] thalassina from Java. Bird Conserv Int 23:91–109. https://doi.org/10.1017/S0959270911000360
Barker MJ (2007) The empirical inadequacy of species cohesion by gene flow. Philos Sci 74:654–665. https://doi.org/10.1086/525611
Barker MJ (2019) Species and other evolving lineages as feedback systems. Philos Theory Pract Biol. https://doi.org/10.3998/ptpbio.16039257.0011.013
Barnett MK (1956) The development of thermometry and the temperature concept. Osiris 12:269–341. https://doi.org/10.1086/368601
Baum DA (2009) Species as ranked taxa. Syst Biol 1:74–86. https://doi.org/10.1093/sysbio/syp011
Bringmann LF, Eronen MI (2016) Heating up the measurement debate: what psychologists can learn from the history of physics. Theory Psychol 26:27–43. https://doi.org/10.1177/0959354315617253
Burfield IJ, Butchart SHM, Collar NJ (2017) BirdLife, conservation and taxonomy. Bird Conserv Int 27:1–5. https://doi.org/10.1017/S0959270917000065
Camargo A, Sites J (2013) Species delimitation: a decade after the renaissance. In: Pavlinov I (ed) The species problem—ongoing issues. InTech, Rijeka, pp 225–247
Carstens BC, Pelletier TA, Reid NM, Satler JD (2013) How to fail at species delimitation. Mol Ecol 22:4369–4383. https://doi.org/10.1111/mec.12413
Cartwright N, Bradburn NM, Fuller J (2011) A theory of measurement. Centre for Humanities Engaging Science and Society (CHESS), Durham
Chang H (2004) Inventing temperature: measurement and scientific progress. Oxford University Press, New York
Conix S (2018) Integrative taxonomy and the operationalization of evolutionary independence. Eur J Philos Sci 8:587–603. https://doi.org/10.1007/s13194-018-0202-z
Conix S (2019) In defence of taxonomic governance. Org Divers Evol. https://doi.org/10.1007/s13127-019-00391-6
Coyne JA, Orr HA (1989) Patterns of Speciation in Drosophila. Evolution 43:362–381. https://doi.org/10.1111/j.1558-5646.1989.tb04233.x
De Queiroz K (1998) The general lineage concept of species, species criteria, and the process of speciation: a conceptual unification and terminological recommendations. In: Howard D, Berlocher S (eds) Endless forms: species and speciation. Oxford University Press, Oxford, pp 57–75
del Hoyo J, Collar NJ (2014) HBW and BirdLife International illustrated checklist of the birds of the world. Lynx Edicions, Barcelona
Donegan TM (2018) What is a species? A new universal method to measure differentiation and assess the taxonomic rank of allopatric populations, using continuous variables. ZooKeys 757:1–67. https://doi.org/10.3897/zookeys.757.10965
Edwards SV (2009) Is a new and general theory of molecular systematics emerging? Evolution 63:1–19. https://doi.org/10.1111/j.1558-5646.2008.00549.x
Ehrlich PR, Raven PH (1969) Differentiation of populations. Science 165:1228–1232. https://doi.org/10.1126/science.165.3899.1228
Ereshefsky M (2011) Mystery of mysteries: Darwin and the species problem. Cladistics 27:67–79. https://doi.org/10.1111/j.1096-0031.2010.00311.x
Faurby S, Eiserhardt WL, Svenning J-C (2016) Strong effects of variation in taxonomic opinion on diversification analyses. Methods Ecol Evol 7:4–13. https://doi.org/10.1111/2041-210X.12449
Flot J-F (2015) Species delimitation’s coming of age. Syst Biol 64:897–899. https://doi.org/10.1093/sysbio/syv071
Fraassen BCV (2008) Scientific representation: paradoxes of perspective. Oxford University Press, Oxford
Fujita MK, Leaché AD, Burbrink FT et al (2012) Coalescent-based species delimitation in an integrative taxonomy. Trends Ecol Evol 27:480–488. https://doi.org/10.1016/j.tree.2012.04.012
Galtier N (2019) Delineating species in the speciation continuum: a proposal. Evol Appl. https://doi.org/10.1111/eva.12748
García-París M, Jockusch EL (1999) A mitochondrial DNA perspective on the evolution of Iberian Discoglossus (Amphibia: Anura). J Zool 248:209–218
Garnett ST, Christidis L (2017) Taxonomy anarchy hampers conservation. Nature 546:25–27. https://doi.org/10.1038/546025a
Godfray HCJ (2002) Challenges for taxonomy. Nature 417:17–19. https://doi.org/10.1038/417017a
Haber MH (2012) Multilevel lineages and multidimensional trees: the levels of lineage and phylogeny reconstruction. Philos Sci 79:609–623. https://doi.org/10.1086/667849
Haber MH (2019) Species in the age of discordance. Philos Theory Pract Biol. https://doi.org/10.3998/ptpbio.16039257.0011.021
Halley, Klicka JC, Clee PRS, Weckstein JD (2017) Restoring the species status of Catharus maculatus (Aves: Turdidae), a secretive Andean thrush, with a critique of the yardstick approach to species delimitation. Zootaxa 4276:387–404. https://doi.org/10.11646/zootaxa.4276.3.4
Hebert P, Gregory TR (2005) The promise of DNA barcoding for taxonomy. Syst Biol 54:852–859. https://doi.org/10.1080/10635150500354886
Hey J, Pinho C (2012) Population genetics and objectivity in species diagnosis. Evolution 5:1413–1429
Isaac NJB, Mallet J, Mace GM (2004) Taxonomic inflation: its influence on macroecology and conservation. Trends Ecol Evol 19:464–469. https://doi.org/10.1016/j.tree.2004.06.004
Khuroo AA, Dar GH, Khan ZS, Malik AH (2007) Exploring an inherent interface between taxonomy and biodiversity: current problems and future challenges. J Nat Conserv 15:256–261. https://doi.org/10.1016/j.jnc.2007.07.003
Lowe WH, Allendorf FW (2010) What can genetics tell us about population connectivity? Mol Ecol 19:3038–3051. https://doi.org/10.1111/j.1365-294X.2010.04688.x
Mace GM (2004) The role of taxonomy in species conservation. Philos Trans R Soc Lond B 359:711–719. https://doi.org/10.1098/rstb.2003.1454
Maddison WP (1997) Gene trees in species trees. Syst Biol 46:523–536. https://doi.org/10.1093/sysbio/46.3.523
Mallet J, Besansky N, Hahn MW (2015) How reticulated are species? BioEssays. https://doi.org/10.1002/bies.201500149
Mari L, Carbone P, Giordani A, Petri D (2017) A structural interpretation of measurement and some related epistemological issues. Stud Hist Philos Sci Part A 65–66:46–56. https://doi.org/10.1016/j.shpsa.2017.08.001
Mayden R (1997) A hierarchy of species concepts: the denouement in the saga of the species problem. In: Claridge M, Dawah H, Wilson RA (eds) Species, the units of biodiversity, systematics association special volume series. Chapman & Hall, London, pp 381–424
Palsbøll PJ, Bérubé M, Allendorf FW (2007) Identification of management units using population genetic data. Trends Ecol Evol 22:11–16. https://doi.org/10.1016/j.tree.2006.09.003
Reiss J (2008) Error in economics: towards a more evidence–based methodology. Routledge, London
Reiss J (2013) Philosophy of economics: a contemporary introduction. Routledge, London
Remsen JV (2015) Book review: HBW and BirdLife International illustrated checklist of the birds of the world volume 1: non-passerines. J Field Ornithol 86:182–187. https://doi.org/10.1111/jofo.12102
Remsen JV (2016) A “rapid assessment program” for assigning species rank? J Field Ornithol 87:110–115. https://doi.org/10.1111/jofo.12142
Rheindt FE, Székely T, Edwards SV et al (2011) Conflict between genetic and phenotypic differentiation: the evolutionary history of a ‘lost and rediscovered’ shorebird. PLoS ONE 6:e26995. https://doi.org/10.1371/journal.pone.0026995
Roux C, Fraïsse C, Romiguier J et al (2016) Shedding light on the grey zone of speciation along a continuum of genomic divergence. PLOS Biol 14:e2000234. https://doi.org/10.1371/journal.pbio.2000234
Schlick-Steiner BC, Steiner FM, Seifert B et al (2010) Integrative taxonomy: a multisource approach to exploring biodiversity. Annu Rev Entomol 55:421–438. https://doi.org/10.1146/annurev-ento-112408-085432
Schuchmann K-L, Weller A-A, Jürgens D (2016) Biogeography and taxonomy of racket-tail hummingbirds (Aves: Trochilidae: Ocreatus): evidence for species delimitation from morphology and display behavior. Zootaxa 4200:83–108. https://doi.org/10.11646/zootaxa.4200.1.3
Sherry D (2011) Thermoscopes, thermometers, and the foundations of measurement. Stud Hist Philos Sci Part A 42:509–524. https://doi.org/10.1016/j.shpsa.2011.07.001
Simpson G (1961) Principles of animal taxonomy. Columbia University Press, New York
Sites JW, Marshall JC (2003) Delimiting species: a Renaissance issue in systematic biology. Trends Ecol Evol 18:462–470. https://doi.org/10.1016/S0169-5347(03)00184-8
Sobel JM, Chen GF, Watt LR, Schemske DW (2010) The biology of speciation. Evolution 64:295–315. https://doi.org/10.1111/j.1558-5646.2009.00877.x
Sterner B (2017) Individuating population lineages: a new genealogical criterion. Biol Philos 32:683–703. https://doi.org/10.1007/s10539-017-9580-4
Sterner BW (2019) Evolutionary species in light of population genomics. Philos Sci. https://doi.org/10.1086/705527
Tal E (2013) Old and new problems in philosophy of measurement. Philos Compass 8:1159–1173. https://doi.org/10.1111/phc3.12089
Templeton (1992) The meaning of species and speciation: a genetic perspective. In: Ereshefsky M (ed) The units of evolution: essays on the nature of species. MIT Press, Cambridge, pp 159–183
Tobias JA, Seddon N, Spottiswoode CN et al (2010) Quantitative criteria for species delimitation. Ibis 152:724–746. https://doi.org/10.1111/j.1474-919X.2010.01051.x
Vallejo-Marín M, Buggs RJA, Cooley AM, Puzey JR (2015) Speciation by genome duplication: repeated origins and genomic composition of the recently formed allopolyploid species Mimulus peregrinus. Evolution 69:1487–1500. https://doi.org/10.1111/evo.12678
Wheeler QD (2005) Losing the plot: DNA “barcodes” and taxonomy. Cladistics 21:405–407. https://doi.org/10.1111/j.1096-0031.2005.00075.x
Wiley EO (1978) The evolutionary species concept reconsidered. Syst Biol 27:17–26. https://doi.org/10.2307/2412809
Willis SC (2017) One species or four? Yes!…and, no. Or, arbitrary assignment of lineages to species obscures the diversification processes of Neotropical fishes. PLoS ONE 12:e0172349. https://doi.org/10.1371/journal.pone.0172349
Willmann R, Meier R (2000) A critique from the hennigian species concept perspective. In: Wheeler QD, Meier R (eds) Species concepts and phylogenetic theory: a debate. Columbia University Press, New York, pp 101–119
Yang Z, Rannala B (2010) Bayesian species delimitation using multilocus sequence data. PNAS 107:9264–9269. https://doi.org/10.1073/pnas.0913022107
Zachos FE (2016) Species concepts in biology: historical developmentm, theoretical foundations and practical relevance. Springer, Basel
Zachos FE (2018) (New) Species concepts, species delimitation and the inherent limitations of taxonomy. J Genet 97:811–815. https://doi.org/10.1007/s12041-018-0965-1
Acknowledgements
I am grateful to Charles Pence, Hugh Desmond, Hardy Schilgen, and the philosophy of biology reading group at the CLPS Leuven for very helpful and detailed comments on earlier drafts of this paper. I also want to thank three anonymous reviewers for their helpful suggestions. Financial support was provided by BOF funding granted by the KU Leuven Onderzoeksraad, Grant 3H160214.
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Conix, S. Measuring evolutionary independence: A pragmatic approach to species classification. Biol Philos 34, 53 (2019). https://doi.org/10.1007/s10539-019-9714-y
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DOI: https://doi.org/10.1007/s10539-019-9714-y