Phylogenetic Analysis of Molecular Data
Phylogenetic Analysis of Molecular Data BOTANY 563
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Systematic Binlngy QRD Svstemahc Biologv m Deerrewew anw Du nut one Species as Ranked Taxa Kevwards Qscholaroui Manuscvlm cemm h pmcmznus criplcenlrzlcnmsyslhinl Page 1 of 44 Systematic Biology RUNNING HEAD SPECIES AS RANKED TAXA COOJVCDU ILCOMA Species as Ranked Taxa 27 DAVID A BAUM 30 Department of Botany University of Wisconsin iMadison 430 Lincoln Dr Madison WI 53 706 32 USA dbaumwisc edu 39 Contact Information 41 David A Baum 44 Dept of Botany 46 430 Lincoln Dr 48 Madison WI 53706 51 Email dbaumwiscedu 53 Tel 6082655385 h 39p39llmr 39 39 39 quot 39 39 COOJVCDU ILCOMA Systematic Biology Page 2 of 44 Page 2 Abstracti Because species names play an important role in scienti c communication it is more important that species be understood to be taxa than that they be equated with functional ecological or evolutionary entities While most biologists would agree that taxa are composed of organisms that share a unique common history two major challenges remain in developing a speciesastaxa concept First grouping in the face of genealogical discordance at all levels in the taxonomic hierarchy how can we understand the nature of taxa Second ranking what criteria should be used to designate certain taxa in a nested series as being species The grouping problem can be solved by viewing taxa as exclusive groups of organisms 7 sets of organisms that form a clade for a plurality of the genome more than any con icting set However no single objective criterion of species rank can be proposed Instead the species rank should be assigned by practitioners based on the semisubjective application of a set of species ranking criteria While these criteria can be designed to yield species taxa that approximately match the ecological evolutionary and morphological entities that taxonomists have traditionally associated with the species rank such a correspondence cannot be enforced without undermining the assumption that species are taxa The challenge and art of monography is to use genealogical and other kinds of data to assign all organisms to one and only one speciesranked taxon Various implications of the speciesasrankedtaxa view are discussed including the synchronic nature of taxa fossil species the treatment of hybrids and species nomenclature I conclude that while challenges remain adopting the view that species are ranked taxa will facilitate a muchneeded revolution in taxonomy that will allow it to better serve the biodiversity informatic needs of the 21st century KEYWORDS J P clquot i ity Gene J Hybridization Monography Phylogenetic nomenclature Species concepts Taxonomy hffp39llmr 39 39 39 quot 39 39 Page 3 of 44 COOJVCDU ILCOMA Systematic Biology Page 3 Considering that species level taxonomy provides the basic reference system for biological diversity it is unfortunate that biologists have failed to establish an agreed upon meaning of the term species Calling a group of organisms a species might be taken to mean that it is an evolutionary unit a lineage a population an ecological entity a morphologically distinct entity or just a group given a formal binomial name One could argue that such imprecision over the meaning of species is to be expected and is not undesirable when meaning is established by language games Pigliucci 2003 This perspective implies that the species category is a cluster concept referring to a set of entities that share a family resemblance rather than being tied to any necessary and sufficient attributes Even if one thinks that family resemblance is the way that meaning is established in everyday discourse in the context of rigorous scientific communication we can aspire to more precision But given the range of connotations of the term how can we settle on a set ofnecessary and sufficient properties of species Although a broad diversity of species concepts have been proposed I would suggest that there is one major axis of variation speciesastaxa versus speciesasfunctionalunits Species astaxon concepts are ones that emphasize the similarities between species and taxa at other ranks and mainly re ect a desire to guide taxonomists in the practice of assigning groups of organisms to species taxa Speciesasfunctionalunits concepts are ones that emphasize the functional cohesion or causal efficacy of species and generally emphasize the role of the term species in evolutionary and ecological theory The clearest way to distinguish these two kinds of concepts is by asking the question What is it about a group of organisms living at one moment that would make them one species as to opposed to two or many or a subset of a single species If the answer is something about their functional integrity for example interbreeding potential or ecological cohesion then the concept is functional By this reasoning the hH p39lmr 39 39 39 COOJVCDU ILCOMA Systematic Biology Page 4 of 44 Page 4 biological Mayr 1969 evolutionary Simpson 1961 Wiley 1978 ecological Van Valen 1976 and cohesion Templeton 1989 species concepts are all functional in outlook If the answer to the question stresses the same kinds of attributes that are used to delimit higher taxa then the species concept is taxic in outlook Thus the phenetic Sneath 1976 morphological Cronquist 1978 diagnosability Cracraft 1983 Nixon and Wheeler 1990 Davis and Nixon 1992 monophyly de Queiroz and Donoghue 1988 and genealogical Baum and Shaw 1995 concepts all use the same grouping criterion for species and higher taxa making them speciesas taxa concepts However some other concepts require some exploration The internodal or Hennigian species concept argues that species are lineages Ridley 1989 At first sight this concept might seem to align with speciesastaxa because modern views of taxa assume that they are like lineages natural chunks of the tree of life However internodal concepts are usually speciesasfunctionalunits concepts because the limits of a lineage at a moment in time are not governed by history morphology or similarity but by functional features Indeed internodal concepts are best viewed as versions of the Evolutionary Species Concept Simpson 1961 Wiley 1978 that stress the temporal extent of species lineages The same can be said of the unified or general lineage species concept de Queiroz 2005 2007 which defines species as separately evolving metapopulation lineages where a metapopulation refers to an inclusive population made up of connected subpopulations de Queiroz 2007 881 Although de Queiroz 1999 2005 2007 argues that monophyly is a valid criterion for recognizing that a metapopulation lineage is separate this does not make monophyly a necessary attribute of metapopulation lineages Rather monophyly is just a secondary feature that is likely to arise if metapopulation lineages have been isolated for long enough Thus the unified species concept is a speciesasfunctionalunits concept hffp39llmr 39 39 39 quot 39 39 Page 5 of 44 COOJVCDU ILCOMA Systematic Biology Page 5 Attempts to reconcile both functional and taxic views under a single umbrella concept are doomed Ifboth kinds of entities were simultaneously covered by a generalpurpose species confusion would reign It would continually be unclear whether the term was being used to refer to taxa understood in various ways or functional entities of various kinds One way to defend pluralism is to suggest that different kinds of species should have different monikers for example 39 39 and I Ereshefsky 1992 Baum 1998 However r r while such terms may help achieve more nuanced communication in evolutionary and ecological theory it is hard to see how these could help in taxonomy It seems unrealistic to plan on developing multiple parallel taxonomies of life one for each kind of species 7 we have a hard enough time maintaining one taxonomic system without trying to juggle two three or more So in the context of taxonomy we should aspire to monism The term species should be applied to groups of organisms based on evidence that they correspond to some particular notion of species Should this be a speciesastaxon or speciesasfunctionalunit concept At their most basic species are taxa assigned the rank of species As a practical reality the discovery of a new species involves two steps first deciding that a group of organisms constitutes a distinct taxon and second deciding that that group is a species rather than a more or less inclusive taxon subspecies genus etc And even after their initial discovery taxa ranked as species may be later recognized at another rank or vice versa Thus the practice of taxonomy implies that species is a rank of taxon thereby supporting the speciesastaxon approach Equating species with taxa can also be defended for theoretical reasons Most modern systematists would agree that taxa are groups of organisms that have a unique common history ie they have the property of monophyly or something like it In that case provided species hH p39lmr 39 39 39 COOJVCDU ILCOMA Systematic Biology Page 6 are also taxa it becomes valid to refer to the position of a species on a phylogeny or the evolutionary relationships of one species to others In contrast if species are functional entities of any sort there is no reason to assume that they will show historical unity in which case species could not be said to occupy a single position on the tree of life So for this reason too species should be viewed as a rank of taxon even if that undermines the assumption that all species are functional units in ecology andor evolution In order to develop a coherent speciesastaxon concept we need a clear understanding of what taxa are Then we can ask what makes some taxa but not others species In this paper I first clarify the concept of a taxon in light of recent advances in analyzing genealogical discordance I then argue that the assignment of taxa to the rank of species cannot be fully objective without undermining the demand that species be taxa The recognition that there is nothing distinctive about the species rank aligns with Darwin s views Mallet 2008 Ereshefsky in press The concept I present is an update to the genealogical species concept Baum and Shaw 1995 except with regards to ranking for which my position is closer to the ideas of Mishler and coworkers Mishler and Donoghue 1982 Mishler and Brandon 1987 Mishler 1999 Fisher et al 2007 However I believe that my formulation adds clarity to previous work by refining the concept of a taxon and hence species based on genealogical exclusivity and by enumerating a set of semisubjective ranking criteria I begin by providing a brief summary of my species concept and then revisit and expand on some important details I end by suggesting that treating species as ranked taxa will help to revolutionize taxonomy so that it can serve modern needs as a repository of biodiversity information hffp39llmr 39 39 39 quot 39 39 Page 7 of 44 Systematic Biology Page 7 EXCLUSIVE GROUPS AND SPECIES RANKING COOJVCDU ILCOMA 11 We can assume that every homologous nucleotide position shared by a group of 13 contemporaneous organisms has a single true treelike history This tree has some reasonably high probability of being identical to that of the two neighboring nucleotide positions However 18 as one increases the spatial distance among nucleotide positions it becomes increasingly likely 20 that different positions will have tracked different histories This problem genealogical discordance poses a signi cant conceptual challenge If different clades can be true for different 25 parts of the genome and if our concept of a taxon is tied to the concept of a clade then different 27 taxa can be true for different parts of the genome Thus if our objective were to base 30 taxonomic decisions on the assignment of organisms to clades genealogical discordance would 32 seem to undermine our endeavor How can we articulate an ontology of taxa that is meaningful 34 even when genealogical discordance applies 37 A set of organisms either forms a clade or does not form a clade on a particular 39 nucleotide position s true tree Therefore there is some actual if unknown proportion of the homologous nucleotide positions for which a particular subset of organisms forms a clade Let 44 us call this proportion the concordance factor of the group of organisms Baum 2007 The 46 concordance factor refers to the probability of drawing a single homologous site at random from each organism and having those organisms form a clade see Baum 2007 for more discussion 51 A specified subset of contemporaneous organisms could be a clade for anywhere between 0 53 and 100 of the genome corresponding to a range of true concordance factors from 00 to 10 hffp39llmr 39 39 39 quot 39 39 COOJVCDU ILCOMA Systematic Biology Page 8 of 44 Page 8 Concordance factors can be estimated from multilocus sequence data sets using Bayesian Concordance Analysis Ane et al 2007 This approach assumes that each locus is a non recombined block consisting of nucleotide positions with a single true genealogy Ifthere is no systematic difference in the length of loci as a function of their true genealogy then the proportion of loci having a clade should equal the proportion of nucleotide positions having the clade This fact predicts that full genomic approaches which have yet to be developed and multilocus approaches will yield similar concordance factor estimates in practice Let us now define an exclusive group as a set of contemporaneous organisms that forms a clade for more of the genome than any con icting ie overlapping set of organisms Thus an exclusive group is a set of organisms whose concordance factor is higher than that of any set of organisms that includes at least one organism from outside the group and some but not all organisms from within group Under this de nition a set of organisms can be exclusive even if it forms a clade for less than 50 of the genome provided that no con icting clade is true of a higher proportion of the genome Therefore this concept of exclusivity while similar in spirit to that proposed by Baum and Shaw 1995 is much more liberal in that it allows one to recognize divergent treelike structures when concordance factors fall below 10 see Baum 2007 for more discussion I propose that taxa should be defined as exclusive groups of organisms Thus assigning an organism to a taxon represents a hypothesis that it forms a clade with all other members of that taxon for more of the genome than any overlapping set of organisms The nature of this taxon concept ensures that taxa so defined will always be hierarchically nested However because exclusivity can apply even when a set of organisms forms a clade for only a small proportion of the genome hierarchical structure and thus taxa may exist well below the level hffp39llmr 39 39 39 quot 39 39 Page 9 of 44 COOJVCDU ILCOMA Systematic Biology Page 9 that is typically associated with the species rank For example a set ofthree siblings might be exclusive while forming a clade for only 25 of their genomes The revised genealogical species concept views species as those taxa among a nested series that are designated as being at the species rank There is no available fully objective ranking criterion for species The closest would be time since common ancestry Hennig 1966 Avise and Mitchell 2007 but different parts of the genome can have different histories and hence different times since common ancestry Furthermore a strict application of a temporal ranking criterion would likely lead to the recognition of species within species and would also likely rank as species some taxa that do not warrant such a designation for other reasons Given the lack of a single objective ranking criterion the best we can do is to recognize that there is some ambiguity in the ranking of taxa but that nonetheless there are certain features that we expect of those taxa ie exclusive groups that are ranked as species These features should each refer to real biological attributes giving them some measure of objectivity However because there are multiple criteria that can be used to rank species Table l and these will sometimes con ict with one another the ranking of taxa as species is best viewed as semi subjective These ranking criteria fall into five general categories biological significance utility predictive power robustness and precedent as outlined below Biological signi cance 7 Species should correspond as closely as possible to units that I A are I J to have y andor 39 importance For example when two or more nonoverlapping taxa occur in sympatry and are not in the process of merging due to interbreeding they should be ranked as separate species Utility 7 The species rank should apply if at all possible to taxa that are internally homogenous can readily be distinguished from other nonnested taxa and have biological hH p39lmr 39 39 39 COOJVCDU ILCOMA Systematic Biology Page 10 of 44 Page 10 properties that give us a reason to talk about them It is also helpful if the degree of phenotypic distinction between species has some degree of constancy within a larger group Predictive power 7 The species rank would generally be applied to taxa about which generalizations can be made One important facet of the ability to generalize about all the organisms within a species is the expectation that they have a common genealogical history for more than a trivial proportion of their genome Thus it would be preferable to recognize as species only those taxa that have a reasonably high concordance factor This is likely to align with being able to make predictions about the biological properties morphology physiology ecology distribution etc of organisms in the species Robustness 7 Because of the importance of maintaining stability of species names taxa assigned the rank of species should ideally be those whose status as exclusive groups is confidently determined What matters is not our confidence that the group forms a clade on a given gene tree but that it forms a clade on more gene trees than any overlapping set of organisms And it doesn t necessarily matter how high the concordance factor is For example a group with an estimated concordance factor of 03 might be acceptable if there is clear evidence that no con icting clade has a concordance factor over 02 Ane et al 2007 describe how Bayesian Concordance Analysis permits one to assess statistical confidence that a particular group of organisms forms a clade for more of the genome that any con icting group Precedent 7 Unless other considerations weigh strongly taxa previously assigned species rank should continue to be recognized By maintaining continuity of usage species ranked taxa become better units for communicating biological information There is a fundamental difference between species grouping which is tied to the objective concept of exclusivity and species ranking which is tied to a set of semisubjective hffp39llmr 39 39 39 quot 39 39 Page 11 of 44 COOJVCDU ILCOMA Systematic Biology Page 11 ranking criteria The question does such and such a group of organisms constitute an exclusive group ie taxon is a question that has a true answer Either it is a taxon or it is not We might be uncertain as to the correct answer and even when we are con dent in our answer we could be mistaken but there is a true answer Consequently scienti c data can be used to arbitrate a dispute as to whether a group of organism is a taxon and thus potentially a species In contrast consider the question is such and such a taxon a species Supposing that it is a taxon as implied in the question there is not an objectively true answer While each ranking criterion relates to a more or less objective property of taxa the species rank is not de ned based on any one criterion but rather is determined by the judicious balancing of multiple potentially con icting considerations Different criteria will often be at odds with one another for example a clade may be geographically and hence reproductively isolated but lack phenetic or ecological distinctiveness from related taxa Furthermore ranking decisions are not made by looking at taxa onebyone but by considering a larger taxon and evaluating the best way to divide it into species such that all organisms are in species Consequently although data can be helpful in resolving a dispute about the species rank there is no underlying ontological claim that can be rigorously tested The species rank is not a hypothesis but a judgment The art of monography is to work within the rigid constraints of genealogical relatedness yet to nd a balance of con icting ranking criteria that gains the support of other specialists and serves the needs of the user community FURTHER IMPLICATIONS hffp39llmr 39 39 39 quot 39 39 COOJVCDU ILCOMA Systematic Biology Page 12 of 44 Page 12 Having now introduced the basics of my genealogical species and taxon concept I will now expand on some issues that I have glossed over In the process I will discuss and counter some possible objections Gene genealogical versus organismic exclusivity 7 The use of genegenealogical exclusivity rather than organismic exclusivity as the core of the taxon and hence species concept deserves explanation Genegenealogical exclusivity refers to genetic ancestry and speci cally to groups that form clades for a plurality of the genome As used here organismic exclusivity refers to descent from common ancestral organisms There are several ways one might formally define organismic exclusivity but Ihave developed with input from E Sober and J Velasco University of Wisconsin 7 Madison a relatively stringent definition A set of contemporaneous organisms M shows organismic exclusivity if there is at least one organism A that is an ancestor of all individuals in M such that A is also a descendant of all the common ancestors shared by any individual in M and any contemporaneous individual outside M Given this definition four sets of contemporaneous organisms in Fig l constitute organismic exclusive groups Because genetic ancestry is constrained by the paths of parentoffspring descent organismic and genegenealogical exclusive groups will usually have identical content So the bracketed groups of organisms in Figure 1 would probably also show genegenealogical exclusivity Therefore a substitution of organismic for genegenealogical exclusivity in the taxon concept would not have major consequences in terms of the groups that would actually hffp39llmr 39 39 39 quot 39 39 Page 13 of 44 COOJVCDU ILCOMA Systematic Biology Page 13 satisfy the concept In both cases there will be a hierarchically nested series of groups satisfying the criterion thus requiring the application of semisubjective ranking criteria Despite the similarity of the two concepts of exclusivity they are not identical and will not always identify the same sets of organisms Of particular importance directional selection acting on loci distributed across the genome can result in genegenealogical exclusivity even in a group that does not show organismic exclusivity Conversely some groups that show organismic exclusivity may nonetheless fail to show genegenealogical exclusivity if patterns of genetic segregation have deviated from Mendelian expectations as could happen by chance or due to selection Given the potential for an occasional discrepancy between the two kinds of exclusivity an unambiguous taxon concept should specify which has priority Although I can see arguments in both directions I favor giving primacy to the gene genealogical criterion Organismic ancestry constrains how genetic ancestry should be structured under Mendelian inheritance and in the absence of selection When the realized patterns of genetic relatedness deviate from expectation Ithink we should recognize taxa based on what actually happened rather than worry about what should have happened In particular it seems preferable to adopt genegenealogical exclusivity which is sensitive to a history of selection rather than organismic exclusivity which is not Additionally genegenealogical exclusivity is more tractable in practice because we can relatively directly evaluate actual genomic ancestry for example using concordance analysis Ane et al 2007 Thus Ibelieve that genegenealogical exclusivity provides a more helpful and more tractable criterion for grouping organisms into species and other taxa Therefore for the remainder of this paper the term exclusivity should be understood to mean gene genealogical rather than organismic exclusivity hffp39llmr 39 39 39 quot 39 39 COOJVCDU ILCOMA Systematic Biology Page 14 of 44 Page 14 Temporal extent 7 The de nition of taxa and hence species adopted here is synchronic taxa are entities composed only of contemporaneous organisms This con icts with the common viewpoint that species are diachronic persisting entities with births at speciation and deaths at extinction or speciation The desire to have species persist through time partly re ects human psychological predispositions the minute something is given a proper name or even just pointedout as a particular entity eg this computer that coffee cup we tend to view it as persisting through time Additionally the history of treating species as functional units tends to tie us to a diachronic view of species However there are good reasons why taxa including species should not be treated as diachronic entities The genealogical de nition of a taxon speci es that the organisms in question are contemporaneous making species and other taxa synchronic entities Can we remove the requirement that organisms be contemporaneous This would make the de nition of a taxon a group of organisms living or dead that forms a clade for a plurality of the genome A minor argument against such a move is that we would be lumping different kinds of relatedness some pairs of organisms are related as ancestor and descendant an asymmetric relationship whereas other pairs are related by common ancestry a symmetric relationship But this heterogeneity does not seem like a devastating problem because the former can be considered as a special case of the latter in which the last common ancestor of a pair of organisms is one of those two organisms Another problem with a diachronic version of exclusivity is that it renders it impossible to place all organisms into a species or any other mandatory rank For example if one decided that exclusive groups should be ranked as species named A and B then any organism that is hffp39llmr 39 39 39 quot 39 39 Page 15 of 44 COOJVCDU ILCOMA Systematic Biology Page 15 ancestral to both A and B could not be in any species because all the cladestaxa of which it is part will include species A and B and thus cannot also be ranked as a species Thus a time extended view of taxa disallows the use of any mandatory rank including species Brummitt 2002 Nonetheless one could do without mandatory ranks So again this issue alone would not invalidate diachronic exclusivity There is one major and so far as I know insurmountable problem with a diachronic version of exclusivity if you include organisms close to branching events then no exclusive groups exist This is because some organisms close to lineage branching events will show equivalent relationships to organisms in different lineages So when you look at the full set of gene trees for all organisms no sets of organisms will show gene genealogical or even organismic exclusivity Including ancestral organisms tends to result in exclusive groups slipping away into a sea of overlapping nonexclusive groups Thus while it would have little effect if the concept of contemporaneous were extended to encompass tens or hundreds of generations the inclusion of more ancient ancestral organisms would make the concept unworkable The fact that we cannot apply the exclusivity criterion to timeextended entities of more than trivial evolutionary duration does not in itself rule out the existence of diachronic species Baum 1998 A synchronic entity can be associated with a diachronic counterpart by connecting successive synchronic slices into diachronic worms The idea is that if we apply a synchronic criterion of individuation in multiple successive instants of time then the synchronic entities in adjacent timeslices can be linked into a timeextended entity Do diachronic counterparts of synchronic species exist hffp39llmr 39 39 39 quot 39 39 COOJVCDU ILCOMA Systematic Biology Page 16 of 44 Page 16 In the original version of the genealogical species concept Baum and Shaw 1995 the species rank was objective corresponding to a concordance factor of 10 This allowed one to imagine connecting the speciesranked groups in each successive slice of time to make a time extended species lineage Baum 1998 However in the revised concept used here the species rank is no longer objective which introduces a signi cant problem Once speciesranked taxa have been delimited in adjacent time slices there is nothing to say that the species rank has been assigned equivalently So there is no conceptually rigorous basis for linking particular taxa in successive slices of time as being continuations of the same diachronic species Once we admit that ranking is nonobj ective then linking synchronic entities into diachronic worms becomes nonobj ective too This means that taxa including species are best viewed as groups of contemporaneous organisms that do not exist through evolutionary time One reason biologists have been troubled by a synchronic view of species is because of a continued commitment to species as causal players in evolution However my explicit objective here is to de ne species as taxa hence products of evolution In this context the lack of diachronic existence is not a problem Indeed it may be a necessary feature of a product of evolution that it lacks diachronic existence Lee and Wolsan 2002 Evolution is an ongoing process that is constantly changing the entities that exist in nature The products of evolution evolve Maybe then it is inevitable that our taxon concept implies only synchronic existence Fossils 7 The synchronic nature of taxa and species poses little practical problem for neontological systematics However my species concept may seem to pose problems for paleontologists Empirically the estimation of concordance factors for fossils poses major perhaps insurmountable problems We are unlikely to have access to molecular data for fossils hffp39llmr 39 39 39 quot 39 39 Page 17 of 44 COOJVCDU ILCOMA Systematic Biology Page 17 organisms making it difficult to rigorously evaluate exclusivity Additionally because species and other taxa are delimited with reference to contemporaneous organisms it will be problematic to establish species status when only a miniscule proportion of the organisms living at a point in time are known and we generally do not know if different fossils were actually contemporaneous At the conceptual level an evolutionary lineage composed of similarlooking and related organisms distributed through time cannot be equated with a species because species as defined here do not exist through time While this implication may jar with prevailing views of species we should ask if it is sufficiently problematic that we should abandon the genealogical conception of taxa Some fossils are deadend branches of the tree of life Fig 2a whereas others are ancestral to living organisms Figs 2bc In the former case there is no real detriment to treating the fossils as though they were living organisms that have remained unchanged for a long time this also applies to recently extinct taxa like dodos we can assign them to taxa including species as though they were extant Can fossils situated on an internal branch Fig 2b be treated similarly This differs from the preceding case in that these fossil taxa are not expected to have any apomorphic traits More importantly if the fossil organisms lived at different times some could be more closely related to descendants than to earlier specimens from the same fossil taxon This becomes even more complex when a fossil is situated at a node Fig 2c In that case different members ofthe fossil taxon could be more closely related to different descendants of that node undermining the unity of the fossil taxon hffp39llmr 39 39 39 quot 39 39 COOJVCDU ILCOMA Systematic Biology Page 18 of 44 Page 18 Given the importance of talking about fossils and their evolutionary kinship I think one should aim to give species names to those fossil organisms that are not lineal ancestors of later fossils or extant organisms Fig 2a 7 although use of a convention to indicate that the species are not extant is warranted However there should be no requirement that every fossil be assigned to a species In particular fossils that are likely to be ancestors Figs 2bc might better be treated using some other conventions to indicate where they fit on the tree of life But given the rarity of fossils that are direct ancestors of living organisms and even more so fossils situated at internal nodes the vast majority of fossils can safely be treated as though they are extant but unchanged Hybridization 7 Hybridization between taxa that were until recently members of distinct taxa has widely been perceived to be a major problem for any phylogenetic species concept and many other concepts as well As a basis for discussion consider a hypothetical example Figure 3a shows a true concordance tree for a set of tips sampled some time in the past when each taxon had a high concordance factor Given that species are just one of a nested series of clades it does not matter for this discussion whether the individual tips in the figure are ranked as species or are grouped with other tips into more inclusive species Figures 3bc show the two coprimary concordance trees Baum 2007 that exist now given that a hybrid individual or hybrid species H was formed by hybridization of organisms that were in C and D in Figure 3a The first issue you might note is that following hybridization no sets of organisms have concordance factors over 50 Hybridization of two tips greatly reduces the concordance factor of not just the hybrids but all taxa that include one but not both parents 7 a phenomenon we may call trickledown discordance The resulting low concordance factors are deceptive 7 a hffp39llmr 39 39 39 quot 39 39 Page 19 of 44 COOJVCDU ILCOMA Systematic Biology Page 19 set of clades with concordance factors of 05 could re ect just two true gene trees differing only in the placement of one hybrid organism ie very little discordance Trickledown discordance is an artifact of trying to summarize a bimodal distribution of genealogical histories with a single statistic This cautions us that concordance factors provide only an imperfect summary of the full distribution of gene histories but it is not relevant to the claim that taxa should be equated with exclusive groups of organisms The second issue to note is that the set of taxa including species we would recognize will differ depending which of the two coprimary trees 3b or 3c we used as a basis for classification Ifwe used tree 3c we would group H with C and could for example rank BCH as a species Ifwe used tree 3b we would group H with D and might recognize DHEF as a species These are quite different classifications raising the question of how either could be defended A pragmatic response is to allow that one or the other scheme be picked at random as the basis for taxon delimitation This will tend to yield taxa that are formally if marginally exclusive For example taxa such as HD HDE and HDEF recognized under tree 2b have low concordance factors but there is no con icting clade that is true of more of the genome Rather con icting clades tend to have equal concordance factors In this case selecting a coprimary concordance tree at random as a basis for classification would not misinform us as to the true genealogical structure However while the arbitrary classification of hybrids with one or the other parent may not create misinformation it does obscure information 7 namely hybrid ancestry If the hybrids could be identified as such the practicalities of which will be discussed shortly the dual affinities of chimeric organisms or taxa could be re ected in taxonomic practice In order to hffp39llmr 39 39 39 quot 39 39 COOJVCDU ILCOMA Systematic Biology Page 20 of 44 Page 20 understand how the ability to identify hybrids would impact taxonomy we need to consider three alternative situations In the first situation hybridization happened a long time ago with subsequent interbreeding among hybrids and their descendants but no backcrossing to either parent In this case we expect organisms of hybrid ancestry to form a clade on almost all gene trees While different gene trees may place the hybrid taxon with one or the other parental taxon the hybrid itself is an exclusive set of organisms In this case we can recognize and name the hybrid just like any other taxon and could thus rank it as a species If its hybrid status were recognized this taxon could be placed in two places in the classi cation once with each parent perhaps with the hybrid symbol being used to indicate its dual parentage In the second situation hybridization has been recent and or recurrent but again there has not been backcrossing with the parents This results in a set of individuals of hybrid ancestry each of which is related to one or the other parental taxon by a different subset of genes In this case the set of hybrid individuals is not an exclusive group and cannot be viewed as a species or any other rank of taxon Instead the individuals are best viewed as a set of hybrid organisms that simultaneously occupy two places on the tree of life Ifthe chimeric nature of these organisms were recognized they could be discounted from the normal rules of classification They would not need to be assigned to species and they could be pruned off concordance trees thereby counteracting trickledown discordance The final situation to consider is one like the preceding except that there has been backcrossing and introgression of genes into the two parental taxa The degree of introgression is potentially variable from a localized hybrid swarm to complete secondary fusion of the two formerly distinct taxa into a single gene pool However regardless of where on this spectrum hffp39llmr 39 39 39 quot 39 39 Page 21 of 44 COOJVCDU ILCOMA Systematic Biology Page 21 they sit neither the two pure parents nor the hybrids nor the set of both parents plus the hybrids will form an exclusive group So what should we do Pruning the complex parental forms plus hybrids as recommended in the preceding situation is not advisable in this case Backcrossing means that the parental taxa have lost their identity 7 they have effectively gone extinct by secondary fusion This means that we cannot list parents when labeling individuals hybrids Therefore instead of just recognizing their hybridity and excluding them from standard classification it would be preferable to diagnose the two historical signals and recognize that the complex represents an admixture of two exclusive taxa We could recognize and name the two virtual pure taxa maybe at the species rank even if all individual organisms were admixtures to some degree The preceding discussion begs the question of how hybrids could be recognized Given a genealogical perspective a hybrid taxon is a set of organisms that occupies more or less symmetrically two spots on the tree of life It is worth stressing that hybrid taxa are here defined based on the distribution of gene genealogies rather than in terms of a particular historical process of formation If for example hybridization occurred but later almost all genetic material from one parent was lost then the taxon may have an evolutionary history of hybridization but it would not be a contemporary hybrid taxon Is there an objective criterion by which hybrid taxa can be identified based on their gene genealogies I am not aware of any fully developed method However I suspect that it might be possible to use an information compactness criterion as in Ane and Sanderson 2005 to see if the full distribution of gene trees can be more efficiently described when a putative hybrid is treated as two virtual taxa that can attach to the rest of the tree in either of two places If this or some other defensible criterion could be developed it would become possible to objectively hffp39llmr 39 39 39 quot 39 39 COOJVCDU ILCOMA Systematic Biology Page 22 of 44 Page 22 identify hybrid individuals and taxa This is important if taxonomy is to deal satisfactorily with some difficult cases of hybridization For this and other reasons an important avenue for future genealogical theory is the development of a theoretical framework for the genealogical identification of hybridity Nomenclature 7 The speciesastaxa concept espoused here is motivated by the view that it is useful to assign some taxa to the rank of species so as to provide points of reference for scientific communication For this goal to be met we must be able to attach names to species ranked taxa in such a way that communication is not impeded To see if this is possible we need to consider in parallel two nomenclatural systems rankbased nomenclature embodied in the traditional codes and phylogenetic nomenclature embodied in the PhyloCode In rankbased nomenclature the content of a species taxon is set by reference to a type and a diagnosis The latter is idealized as a list of characters that differentiate the species from its closest relatives but it does not provide an essentialist de nition of the species Rather a diagnosis is provided as a window into the thinking of the name s author Thus as with other taxa in rankbased nomenclature the meaning of a species name is basically determined just by reference to a type and the rank of species The question Is organism X in species y is answered by asking if X is in the species that includes the type specimen of y Given the concept of species advocated here species are taxa While not clades in the simplistic sense of monophyletic groups for the whole genome taxa are clades in the looser sense of forming clades for a plurality of the genome Thus the application of a name to a species taxon can be achieved using the same kinds of phylogenetic definition that are used to attach names to other clades de Queiroz and Gauthier 1990 de Queiroz and Gauthier 1992 hffp39llmr 39 39 39 quot 39 39 Page 23 of 44 COOJVCDU ILCOMA Systematic Biology Page 23 For example one could de ne the speciesranked taxon Homo sapiens as including all extant and recent historical organisms that form an exclusive group that includes Charles Darwin say but not certain designated specimens of chimpanzees bonobos or gorillas The use of branch based nodebased or other kinds of phylogenetic de nition instead of or in addition to diagnoses would certainly go some way towards improving the clarity of species taxonomy While genealogical species can be named under the rankbased codes such a system of nomenclature is not optimal because it is premised on ranks including the rank of species being objectively real Under the rankbased codes the association of a species name with a clade will last only so long as that clade continues to be ranked as a species For example imagine that we have provided a nodebased de nition of a clade that includes some horned animals within Equus and have assigned this clade the rank of species giving it the name E unicornus Suppose that a clade that is sister to E unicornus is later discovered and that organisms in this new clade are indistinguishable from members of E unicornus If it were judged necessary to assign the species rank to the larger clade that includes both unicornus and the newly found organisms this expanded species would have the name E unicornus because it is a species including the type of E unicornus In the process the original E unicornus clade has been deprived of its name This shows that under rankbased nomenclature changing rank assignment results in a name applying to a new clade 7 even when the clade it originally applied to remains a valid exclusive taxon Given that phylogenetic nomenclature with its emphasis on phylogenetic relationships is so well aligned with the genealogical species concept it is unfortunate that the current version of the PhyloCode wwwphylocodeorg forbids one from treating species as ranked exclusive taxa Dayrat et al 2008 Articles 3 and 21 of the PhyloCode stipulate that species names are hffp39llmr 39 39 39 quot 39 39 COOJVCDU ILCOMA Systematic Biology Page 24 of 44 Page 24 governed by the traditional ranked codes Furthermore species epithets cannot be converted into phylogenetically de ned clade names Art 109 A clade name may not be converted from a preexisting speci c or infraspeci c epithet ICBN and BC or a speci c or infraspeci c name ICZN At rst glance you might think that the reason that the PhyloCode excludes species is that species is a rank and the PhyloCode is incapable of handling ranks However this is not the case Phylogenetic nomenclature is not rankbased but neither is it rankfree de Queiroz 1997 as made clear in note 312 of the PhyloCode This code does not prohibit discourage encourage or require the use of taxonomic ranks To illustrate how it would be possible to treat species as a rank of clade within the framework of phylogenetic nomenclature consider a hypothetical phylogeny with 12 tips each corresponding to an exclusive group of organisms from a single population Fig 4 These and all clades in this tree have been named Figure 4a shows an original classi cation that achieves exhaustive assignment of all 12 tips to three ranks species indicated by a lower case rst letter genus indicated with an asterisk and family indicated with a plus sign Given this classi cation it might be convenient to refer to organisms by reference to the genus and species clades to which they are assigned yielding pseudobinomials for example Tardz39s magm39 ca and Vogon horridus It should be stressed that the genus name is used merely as a partial clade address and is not part of the species name as it would be in rankbased nomenclature Now suppose that a subsequent authority while accepting the same phylogenetic relationships concluded that all the terminal populations should be ranked as species This would not change the name of any clade but now the annotation of species rank in my example the use of lowercase shifts to the new speciesranked clades Fig 4b For the sake of hffp39llmr 39 39 39 quot 39 39 Page 25 of 44 COOJVCDU ILCOMA Systematic Biology Page 25 illustration suppose that the same author also shifted the genus rank 7 splitting Vogon into Ovalis and Ultra Now under this new classi cation the names of species have changed especially when combined with their generic clade address eg Tardz39s magm39fzca has been split into T angustifolia and T bellissima Vogon ovalz39s has been split into Ovalis liczfolia and O grandz39 ora This shows the undesirability of changing rank assignments whimsically which is why precedent is such an important ranking criterion However although the names of species genera etc have changed the composition and name of every taxon has remained stable This example illustrates the point that phylogenetic nomenclature can in principle accommodate ranks including the rank of species and that it does so in such a way that rank is nomenclaturally neutral So why does the PhyloCode exclude species names Some years ago there was division among proponents of phylogenetic nomenclature as to whether species names should comprise just species epithets uninomials or a fusion of the traditional generic names and epithets Cantino et al 1999 But this dispute has been largely resolved in favor of uninomials primarily due to some empirically worked out examples Dayrat 2005 Dayrat and Gosliner 2005 Instead the decision to exclude species from the PhyloCode rested on practical concerns and one strong philosophical position A number of practical reasons have been put forward for why species names should not be included in the PhyloCode Dayrat et al 2008 Most obviously the current version of the PhyloCode forbids the same name to be used for more than one clade This rule would need to be removed if species epithets were converted into clade names because so many traditionally recognized species share the same epithet Wolsan 2007 Some people fear that systematic communication would be impaired if homonyms were allowed I believe however that we can I39 I J 39 39 easrly J us1ng 1 information andor partial clade addresses So hffp39llmr 39 39 39 quot 39 39 COOJVCDU ILCOMA Systematic Biology Page 26 of 44 Page 26 I do not believe that homonymy is such a problem and nor do I believe that this or any other practical concern motivated the decision to exclude species from the PhyloCode The core reason that the PhyloCode relinquished species was because the individuals who drafted the document hold that species and clades are inherently different kinds of taxa The PhyloCode articulates such a position quite explicitly Note 311 In this code the terms quotspeciesquot and quotcladequot refer to different kinds of biological entities not ranks Similarly in defending the treatment of species names in the PhyloCode Dayrat et al 2008 state Clades and species are regarded as kinds of biological entity under the PhyloCode They are not ranks They go further and assert that p 511 Under the PhyloCode a species is defined as a segment of a populationlevel lineage that is evolving separately from other such population lineages In effect the PhyloCode has adopted the Unified or General Lineage species concept of de Queiroz 1998 2005 2007 As discussed earlier this is a speciesasfunctionalunits concept making it incompatible with the taXic view advocated here Ithink it is a mistake to configure the PhyloCode around a single speciesasfunctionalunits concept It seems like a major failing of the PhyloCode that it makes it impossible to attach species names to phylogenetically defined clades The best you could do would be to name clades that you wished to rank as species within the traditional codes and then treat them within the PhyloCode But because the name is not attached to the clade but to the rank of species there would not be a stable connection between the name and the clade which is the whole point of phylogenetic nomenclature It is ironic that the only nomenclatural system that allows one to treat species as clades is rankbased nomenclature which regrettably treats ranks as though they were objectively real hffp39llmr 39 39 39 quot 39 39 Page 27 of 44 COOJVCDU ILCOMA Systematic Biology Page 27 CONCLUSIONS AND PROSPECTS Given the lack of an objective speciesranking criterion that can place all organisms in speciesranked taxa I have here argued for treating species as a semisubjective rank The idea is that having identi ed a set of taxa that are hypothesized to be exclusive taxonomists should assign taxa to the species rank based on judicious compromises among a set of potentially con icting criteria Under this approach while many species will correspond to functional units in ecology andor evolution it should never be assumed that a speciesranked taxon has functional importance There are two main responses to the lack of an objective species rank The rst is to argue that since species are not distinct from other taxa we gain nothing by using the concept of species for a kind of taxon Instead we should adopt a speciesasfunctionalunits concept This has the advantage that one could then aspire to an objective ranking criterion for species Lee 2003 not that any objective ranking criterion has been identi ed for any speciesasfunctional units concept But as I argued in the introduction de ning species as functional units forgets that species exist in the same hierarchy of named groups as other taxa and that we want to believe that each species occupies a unique position on the tree of life The second response is to abandon the species category entirely if it is just taxa all the way down why pick out one taxon for special attention eg Mishler 1999 Pleijel and Rouse 2000 Fisher et al 2006 Here Iwill argue that we need the species rank not because it is objective but because it and other mandatory ranks provide informatic reference points that facilitate effective communication about biological diversity hffp39llmr 39 39 39 quot 39 39 COOJVCDU ILCOMA Systematic Biology Page 28 of 44 Page 28 Phylogenetic taxonomy provides a reference system for biological diversity analogous to longitude and latitude in geography Both reference systems need a single unambiguous criterion for assigning a unit geographic feature or organism to a place in the system This is why the coexistence of two competing longitudinal reference points at Paris and Greenwich was not viable in the long run Similarly systematics has now largely adopted a single reference system evolutionary relatedness as a basis for defining where an organism fits in the classificatory structure But why do we need the species rank Again consider the analogy to the geographic coordinate system The coordinates of Madison Wisconsin will generally be reported as 43 N 89 W Doing so places Madison within a 1 square providing a useful starting point for locating this city We could provide coordinates within 01 431 N 894 W 001 4309 N 8937 W 2 44 N 90 W or any arbitrary level of accuracy However the degreesquare provides a conventionally agreed upon firstorder summary of the location of geographic feature The species rank can be viewed similarly assigning an organism to a species answers the question where does this organism fit on the tree of life to a conventionally agreed upon if not explicitly defined level of accuracy Likewise assigning organisms to genera answers the same question but with lower precision and assigning organisms to subspecies does so with greater precision A significant difference between the geographic and taxonomic coordinate system is that whereas geographic space has an unambiguous scale in units of degrees taxonomic space is less readily parameterized One might wish to use time since common ancestry but different parts of the genome share common ancestry at different times in the past One might wish to use degree of phenotypic differentiation but phenetic similarity cannot be captured on any one true scale Farris 1982 Thus the scale of relatedness is less easily defined than longitude and latitude hffp39llmr 39 39 39 quot 39 39 Page 29 of 44 COOJVCDU ILCOMA Systematic Biology Page 29 Nonetheless while we cannot readily de ne the size of the phylogenetic neighborhood encapsulated by the species rank it will tend to be a smaller neighborhood than would be designated by the genus rank and so on Maybe in the distant future we will have new ways to instantly communicate a detailed tree picture without having to name taxa But for the time being the only way to tell somebody where an organism ts on the tree of life is to name taxa of which it is a part But there are often too many taxa to name so we need certain ranks that are established as shared reference points for easy communication Among these the species rank has historically been the most important For that reason systematics without the species rank is hard to imagine The species debate is tiresome which is why there have been so many calls to set it aside or to agree to disagree Pigliucci 2003 de Queiroz 2005 Hey 2006 However the species debate is not just academic How we think about species has a very real impact on how taxonomy works And it is hard to look at the status of taxonomy and conclude that the field is in good shape We face a crisis of extinction and habitat destruction which can only be kept track of through taxonomic data Yet the rate at which taxonomic data are generated for example the rate at which new taxa are described and named has barely changed in the last hundred years This is despite the ready availability of powerful computers and increasingly sophisticated and comprehensive databases of 39 39 r39 39 and 39 quot quot J 39 39 data While other informationrich sciences such as geography and genomics have made huge strides taxonomy is largely the same as it was 100 years ago Recent imp v 3 in 39 39 r 39 quot 39 39 and data storage are beginning to have an impact Penev et al 2008 However I believe that a more pragmatic and streamlined approach to species taxonomy and nomenclature has the potential to help break this logjam and allow taxonomy to truly enter the information age hffp39llmr 39 39 39 quot 39 39 COOJVCDU ILCOMA Systematic Biology Page 30 Genealogical history provides the one universal feature of all organisms Therefore we should build a database that maintains information on the inferred relationships of very many placeholder organisms tied to raw molecular data and a database of phylogenetic clade definitions and rank assignments With such a resource taxa could be named consistently and it would be easy using molecular data to quickly determine the taxonomic neighborhood of an unidentified organism Furthermore taxonomists would no longer need to publish monographic treatments in the conventionally laborious way 7 they would just update the databases by adding additional placeholder organisms increasing the accuracy of the genealogical data assigning names to newly discovered taxa and refining ranking so that nearly all living organisms are assigned to species Such a streamlined structure would be much more democratic and efficient than anything we have today Just as any scientist can deposit and annotate a sequence in GenBank subject to editorial oversight so too would a simple genealogically based database allow many more scientists and amateurs to contribute to the bioinformatic infrastructure As a result taxonomy could better serve the needs of scientists policymakers and the public To achieve the goal of converting taxonomy into a modern open information science it is necessary that the concept of species be moved once and for all out of the realm of mechanistic evolutionary biology and kept fully within systematics If species status depends on something different than relationships then we in ate the kinds of data that need to be kept track of and broaden the set of scientists who need to participate in species grouping and ranking Furthermore if species were defined as functional entities or anything but a rank of taxon then we would have to complicate the system by allowing species to overlap in content with taxa Within the framework of speciesastaxa it is also important to give up on the idea that there is an objective way to rank species taxa Once systematists accept that species status is a semi h p39llmr 39 39 39 quot 39 39 Page 31 of 44 COOJVCDU ILCOMA Systematic Biology Page 31 subjective decision they may be less inclined to revise the ranking decisions of previous workers and focus instead on evaluating the exclusivity of species and other taxa By advocating a shift to monistic grouping based on exclusivity and semisubjective ranking I hope that in some small way this paper will help systematics to evolve into the sophisticated information science that it needs to become ACKNOWLEDGMENTS I would like to thank the following individuals who provided helpful discussion and or constructive criticism of the paper Cecile Ane Marc Ereshefsky Matt Haber Marshal Hedin Margaret Koopman Michael Lee James Mallet Elliott Sober Stacey Smith Joel Velasco Kandis Elliot helped prepare artwork I gratefully acknowledge funding from John Simon Guggenheim Foundation and support from the National Science Foundation DEB0416096 for empirical work that helped shape these ideas hffp39llmr 39 39 39 quot 39 39 COOJVCDU ILCOMA Systematic Biology Page 32 of 44 Page 32 REFERENCES Ane C B Larget D A Baum S D Smith and A Rokas 2007 Bayesian estimation of concordance among gene trees Molecular Biology and Evolution 24412426 Avise J C and D Mitchell 2007 Time to standardize taxonomies Syst Biol 56 130133 Baum D A 1998 Individuality and the existence of species through time Syst Biol 47641 653 Baum D A 2007 Concordance trees concordance factors and the exploration of reticulate genealogy Taxon 56417426 Baum D A and K L Shaw 1995 Genealogical perspectives on the species problem Pages 289303 in Experimental and molecular approaches to plant biosystematics P C Hoch and A G Stephenson eds Missouri Botanical Garden Press St Louis Brummitt R K 2002 How to chop up atree Taxon 513141 Cantino P D H N Bryant K De Queiroz M J Donoghue T Eriksson D M Hillis and M S Y Lee 1999 Species names in phylogenetic nomenclature Syst Biol 48790807 Cracraft J 1983 Species concepts and speciation analysis Pages 159187 in Current Ornithology R Johnston ed Plenum Press New York Cronquist A 1978 Once again what is a species Pages 320 in Biosystematics in Agriculture J A Ramberger ed Allanheld and Osmun Monclair NJ Davis J I and K C Nixon 1992 Populations genetic variation and the delimitation of phylogenetic species Syst Biol 41421435 Dayrat B 2005 Advantages of naming species under the PhyloCode An example of how a new species of Discodorididae Mollusca Gastropoda Euthyneura Nudibranchia Doridina may be named Marine Biol Res 1216232 hffp39llmr 39 39 39 quot 39 39 Page 33 of 44 COOJVCDU ILCOMA Systematic Biology Page 33 Dayrat B P D Cantino J A Clarke and K De Queiroz 2008 Species names in the PhyloCode The approach adopted by the International Society for Phylogenetic Nomenclature Syst Biol 57507514 Dayrat B and T M Gosliner 2005 Species names and metaphyly a case study in Discodorididae Mollusca Gastropoda Euthyneura Nudibranchia Doridina Zool Scr 34 199224 de Queiroz K 1997 The Linnaean hierarchy and the evolutionization of taxonomy with emphasis on the problem of nomenclature Aliso 15125144 de Queiroz K 1998 The general lineage concept of species species criteria and the process of speciation A conceptual uni cation and terminological recommendations Pages 5775 in Endless Forms Species and speciation D J Howard and S H Berlocher eds Oxford University Press New York de Queiroz K 2005 Different species problems and their resolution Bioessays 2712631269 de Queiroz K 2007 Species concepts and species delimitation Syst Biol 56879886 de Queiroz K and M J Donoghue 1988 Phylogenetic systematics and the species problem Cladistics 4317338 de Queiroz K and J Gauthier 1990 Phylogeny as a central principle in taxonomy Phylogenetic definitions of taxon names Syst Zool 39307322 de Queiroz K and J Gauthier 1992 Phylogenetic taxonomy Ann ReV Ecol Syst 23449 480 Ereshefsky M 1992 Eliminative pluralism Phil Sci 59671690 Ereshefsky M In press Darwin and the nature of species in 11 futuro di Darwin La specie C L ed Turin PrintingPublishing Union Turin hffp39llmr 39 39 39 quot 39 39 COOJVCDU ILCOMA Systematic Biology Page 34 of 44 Page 34 Farris J 1982 The logical basis of phylogenetic analysis Pages 736 in Advances in cladistics Proceedings of the second meeting of the Willi Hennig Society N Platnick and V Funk eds Columbia University Press New York Fisher K M D P Wall K L Yip and B D Mishler 2007 Phylogeny ofthe Calymperaceae with a rankfree systematic treatment Bryologist 1104673 Hennig W 1966 Phylogenetic systematics University of Illinois Press Urbana IL Hey J 2006 On the failure ofmodern species concepts Trends Ecol Evol 21447450 Lee M and M Wolsan 2002 Integration individuality and species concepts Biol Phil 17 65 1660 Lee M S 2003 Species concepts and species reality salvaging a Linnaean rank J Evol Biol 16 179188 Mallet J 2008 Hybridization ecological races and the nature of species empirical evidence for the ease of speciation Philos Trans R Soc Lond B 363 297172986 Mayr E 1969 Principles of Systematic Zoology Harvard University Press Cambridge MA Mishler B D 1999 Getting Rid of Species Pages 307316 in Species New interdisciplinary essays R Wilson ed MIT Press Cambridge MA Mishler B D and R N Brandon 1987 Individuality pluralism and the phylogenetic species concept Biol Phil 2397414 Mishler B D and M J Donoghue 1982 Species concepts a case for pluralism Syst Zool 3 1491503 Nixon K C and Q D Wheeler 1990 An ampli cation of the phylogenetic species concept Cladistics 6211223 hffp39llmr 39 39 39 quot 39 39 Page 35 of 44 COOJVCDU ILCOMA Systematic Biology Page 35 Penev L T Erwin Thompson F Christian HD Sues M S Engel D Agosti R Pyle M Ivie T Assmann T Henry J Miller N B Ananjeva A Casale W Lourenco S Golovatch HP Fagerholm S Taiti M AlonsoZarazaga and E van Nieukerken 2008 ZooKeys unlocking Earth s incredible biodiversity and building a sustainable bridge into the public domain From printbased to webbased taxonomy systematics and natural history ZooKeys 1 17 Pigliucci M 2003 Species as family resemblance concepts the dissolution ofthe species problem Bioessays 25596602 Ridley M 1989 The cladistic solution to the species problem Biol Phil 4116 Simpson G G 1961 Principles of Animal Taxonomy Columbia University Press New York NY Sneath P H A 1976 Phenetic taxonomy at the species level and above Taxon 25437450 Templeton A R 1989 The meaning of species and speciation a genetic perspective Pages 3 27 in Speciation and its consequences D Otte and J Endler eds Sinauer Sunderland MA Van Valen L 1976 Ecological species multispecies and oaks Taxon 25233239 Wiley E 1978 The evolutionary species concept reconsidered Syst Zool 271726 Wolsan M 2007 Naming species in phylogenetic nomenclature Syst Biol 5610111021 hffp39llmr 39 39 39 quot 39 39 COOJVCDU ILCOMA Systematic Biology Table 1 Proposed species ranking criteria Page 36 Taxa within species Species taxa Taxa including multiple species Biologically meaningful Ecologically identical to close relatives Not Jof 39 39 quot Ecologically distinct from close relatives Not distinct subgroups When cooccurring with close relatives interbreeds with them When close relatives are not in sympatry interbreeding is possible and leads to fit offspring Subgroups can interbreed with each other to produce f1t offspring r J of 39 39 quotJ distinct subgroups When cooccurring with close relatives does not interbreed with them When close relatives are not in sympatry interbreeding is impossible or possible but yields unfit offspring Subgroups can interbreed with each other to produce f1t offspring Ecologically distinct from close relatives Composed of ecologically distinct subgroups When cooccurring with close relatives does not interbreed with them When close relatives are not in sympatry interbreeding is impossible or possible but yields un t offspring Some subgroups cannot interbreed with each other to produce f1t offspring Utility Phenotypically indistinguishable no fixed differences from closely Phenotypically distinct with fixed differences from closely related taxa for hH p39lmr Phenotypically distinct with fixed differences from closely related taxa for Page 36 of 44 Page 37 of 44 COOJVCDU ILCOMA Systematic Biology Page 37 related taxa or if distinct then major traits traits that by minor traits traits that do diagnose species in related not diagnose species in related groups Without phenotypically distinct subgroups or subgroups differentiated by minor traits groups Without phenotypically distinct subgroups or subgroups differentiated by minor traits major traits traits that diagnose species in related groups With phenotypically distinct subgroups that are differentiated by major traits Predictive Power Concordance factor low Subgroups with low concordance factors Concordance factor high Subgroups with low concordance factors Concordance factor high Some subgroups with high concordance factors Robustness Not confident that concordance factor is greater than that of a con icting group No or few subgroups for which we can be confident that the concordance factor is greater than that of con icting groups Confident that concordance factor is greater than that of a con icting group No or few subgroups for which we can be confident that the concordance factor is Confident that concordance factor is greater than that of a con icting group Some subgroups for which we can be confident that the concordance factor is greater greater than that of con icting than that of con icting groups groups Precedent hH p39lmr COOJVCDU ILCOMA Systematic Biology Page 38 Not traditionally 1 species species y 39 as Not traditionally recognized as species hH p39lmr Page 38 of 44 Page 39 of 44 COOJVCDU ILCOMA Systematic Biology Page 39 FIGURE LEGENDS FIGURE 1 A hypothetical pedigree to illustrate the concept of organismic exclusivity Circles represent individual organisms each connected by lines to two parents in the preceding lower generation For each of the four organismically exclusive groups composed only of organisms in the most recent generation one ancestral organism M is marked This organism has the property of being both an ancestor of all living members of the exclusive group and of being a descendant of all ancestors shared by members of the group and any contemporaneous organisms outside the group FIGURE 2 The classi cation of fossils alongside living organisms Whether fossils are extinct terminal branches Fig 2a portions of internal branches Fig 2b or organisms drawn from nodes Fig 2c they can be treated as though they are extant organisms that have not changed since the time of fossilization Only in the first case will multiple fossil organisms constitute an exclusive group relative to living taxa FIGURE 3 Concordance trees before and after hybridization 3a Before hybridization almost all of the genome has tracked the same treelike history as shown by clade concordance factors of 0910 Hybridization of tips C and D to yield a new taxon H generates two coprimary concordance trees Figs 3bc one with H sister to C and one with it sister to D All clades that include one but not both parental taxa C and D have their concordance factors reduced by half as a result of hybridization a phenomenon called trickledown hybridization hffp39llmr 39 39 39 quot 39 39 COOJVCDU ILCOMA Systematic Biology Page 40 of 44 Page 40 FIGURE 4 Phylogenetic nomenclature with species as ranked clades It is assumed that all tips taxa and clades have been attached to names using clade de nitions but that in the two versions different clades are assigned to different ranks Taxa assigned to the species rank are written in lowercase whereas taxa at all other ranks above and below species have their rst letter capitalized Genera are marked with an asterisk and families with a plus sign Note that despite changing ranks all clades have the same names in the two cases h 39p39llmr 39 39 39 quot 39 39 Page 41 of 44 OmNCDO lPOON I Systematic Biology I 3 I 2 I I I N N M 249 II It s gmgze N 39 N quot N kg FIGURE 1 A hypothetical pedigree to illustrate the concept of organismic exclusivity Circles represent individual organisms each connected by lines to two parents in the preceding lower generation For each of the four organismically exclusive groups composed only of organisms in the most recent generation one ancestral organism M is marked This organism has the property of being both an ancestor of all living members of the exclusive group and of being a descendant of all ancestors shared by members of the group and any contemporaneous organisms outside the group 60x111mm 600 x 600 DPI httpllmcmanuscriptcentralcomlsystbiol 00lCDO lIgtOONA Systematic Biology a 9 f fossil b 9 I fossil c 9 fossil FIGURE 2 The classification of fossils alongside living organisms Whether fossils are extinct terminal branches Fig 2a portions of internal branches Fig 2b or organisms drawn from nodes Fig 2c they can be treated as though they are extant organisms that have not changed since the time of fossilization Only in the first case will multiple fossil organisms constitute an exclusive group relative to living taxa 53x133mm 600 x 600 DPI httpllmcmanuscriptcentralcomlsystbiol Page 42 of 44 Page 43 of 44 Systematic Biology 1 2 3 4 5 6 7 8 a A 9 100 10 100 B 11 C 12 1 090 D 15 090 E 16 100 F 17 18 G 19 20 A 21 b 050 325 050 B 24 C 25 D 26 050 27 045 H 28 045 E 29 30 050 F 31 32 G 33 34 A 33 C 050 B 37 050 H 38 050 39 C 40 41 045 D 2125 045 E 44 045 F 45 46 G 47 48 FIGURE 3 Concordance trees before and after hybridization 3a Before hybridization almost all of the genome has tracked the same tree like history as shown by clade concordance factors of 09 49 50 10 Hybridization of tips C and D to yield a new taxon H generates two coprimary concordance trees Figs 3b c one with H sister to C and one with it sister to D All clades that include one but 51 not both parental taxa C and D have their concordance factors reduced by half as a result of 52 hybridization a phenomenon called trickle down hybridization 53 38X121mm 600 x 600 DPI 54 55 56 57 58 59 60 httpImcmanuscriptcentralcomlsystbiol OOICDO IPOONA Systematic Biology Page 44 of 44 a 0 0 quot0 0 19 39 390 0 8 09 046 5960 60 39amp390 3 quot508 4 0 00639 9 00 qo v 6 d 9 9 5 lt6 6 0 0 9 9 0 magni ca novus ovais Perrieri quinquefolia Ruber Simplex Tardis Ultra Vogon UMu b 0 0 a 99 xx 9quot o o Lo Magni ca Novus Ovalis Perrieri Quinquefolia Ruber Simplex Tardis Ultra Vogon UMu FIGURE 4 Phylogenetic nomenclature with species as ranked clades It is assumed that all tips taxa and clades have been attached to names using clade definitions but that in the two versions different clades are assigned to different ranks Taxa assigned to the species rank are written in lowercase whereas taxa at all other ranks above and below species have their first letter capitalized Genera are marked with an asterisk and families with a plus sign Note that despite changing ranks all clades have the same names in the two cases 117x136mm 600 x 600 DPI httplmcmanuscriptcentracomlsystbio