Tree Thinking and Species Delimitation: Guidelines for Taxonomy And

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Mammalian Biology 81 (2016) 185–188

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Mammalian Biology

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Editorial

Tree thinking and species delimitation: Guidelines for taxonomy and

phylogenetic terminology

Frank E. Zachos

Natural History Museum Vienna, Mammal Collection, Burgring 7, Vienna 1010 Austria

a r t i c l e i n f o a b s t r a c t

Article history: By tradition, phylogenetic trees are presented in such a way that species-poor taxa are placed on the

Available online 22 October 2015

left side and their more diverse sister taxa on the right (usually with humans on the far right). This

often leads to reading the tree as a “ladder of progress” from left (allegedly primitive, basal or even

Keywords:

ancestral) to right (allegedly advanced, derived, descendant). Although biologically and logically wrong

Phylogenetic trees

and often bemoaned, the evolutionary literature teems with language perpetuating this phylogenetic

“Primitive lineage fallacy”

misconception. Likewise, the splitting of one into two or more species based on different versions of

Scala naturae

the Phylogenetic Species Concept has recently found a growing number of adherents, resulting, in the

Species concepts

eyes of many, in a trivialization of the species category (“taxonomic inﬂation”). This editorial brieﬂy

Species splitting

summarizes these phylogenetic and taxonomic issues and provides guidelines to authors submitting

their studies to Mammalian Biology in order to avoid errors in phylogenetic discussions and to do justice

to the fundamental nature of species in biology.

Introduction points and guidelines will be given. None of the points mentioned

here are novel insights (for tree interpretation, see Baum et al. 2005;

This editorial is aimed at authors submitting their papers to Omland et al. 2008; there is even a very similar editorial to this one,

Mammalian Biology. We receive quite a number of manuscripts published for the same reasons: Krell and Cranston 2004; for the

dealing with phylogenetic relationships among mammal taxa species debate, the list of publications is all but inﬁnite, cf. Heller

and/or the splitting and description of (new) mammalian species. et al., 2013, 2014; Zachos et al. 2013a; Zachos 2015, in press; for

Most of these papers are good studies, reporting methodologically an opposing view, see Groves 2013; Cotterill et al. 2014). How-

sound analyses and results and drawing appropriate conclu- ever, the same issues and misconceptions arise again and again and

sions from them. There are, however, even in otherwise good are perpetuated in quite a number of papers, so that emphasis and

studies, often very speciﬁc shortcomings, errors or inconsisten- reinforcement of the guidelines below are still needed. Authors sub-

cies. With respect to phylogenetics, they usually result from an mitting phylogenetic and taxonomic papers to Mammalian Biology

erroneous interpretation of trees as “ladders of progress” result- should follow them whenever possible.

ing in, subsequently, phylogenetically inappropriate terminology

(“higher”, “lower”, “basal” and “ancestral” groups). In taxonomy

and species splitting/description, matters are more complicated Phylogenetic trees and how not to read them

and less straightforward, but using monophyly/paraphyly of gene

trees or mere diagnosability as species criteria will inevitably lead Phylogenetic trees depict evolutionary relationships among

to taxonomic inﬂation (Isaac et al. 2004). This kind of taxonomic taxa. In cladograms, the only information conveyed is the topol-

proliferation is strongly discouraged here, and at the very least, ogy itself, i.e. the succession of branching events resulting in a

authors should explicitly name their criteria for species status (i.e. nested pattern of relationships. Other kinds of phylogenetic trees

the species concept adopted). Both topics are too complex to be cov- also contain information on evolutionary rates (depicted by branch

ered in detail in an editorial like this, and below only a few general lengths, phylograms) or absolute time (chronograms). In any case,

it never makes a difference which taxa are drawn on the right side

of the tree and which on the left (the same holds for the upper

and lower sides in horizontal trees). Relationships (i.e. the recency

E-mail address: [email protected] of common ancestors) are only represented by the succession of

http://dx.doi.org/10.1016/j.mambio.2015.10.002

186 Editorial / Mammalian Biology 81 (2016) 185–188

splitting events, and therefore, in a vertical tree, only the y-axis A)

(time) contains information. The x-axis does not contain directional platypus kangaroo anteater aardvark deer mouse human

information, i.e. whether a group is more basal than or ancestral

to another! (In horizontal trees, it is the other way around, but I

will only discuss vertical trees as shown in Fig. 1). Phylogenetic

trees consist of branching lineages, each node (unless it is a poly-

tomy) gives rise to two sister taxa. Sister taxa are, by deﬁnition, of

the same age, and none of them can be more basal than or even

ancestral to the other. Which of the two is depicted on the right

and which on the left side is irrelevant and just a matter of con-

vention or, perhaps more precisely, tradition. The latter has it that

species-poor lineages (or those falsely deemed more “primitive”)

are usually shown on the left side, the species-rich sister taxa on 1

the right (“ladderize right” trees). This invites a common miscon-

me axis No direconal informaon! (illusory noon of progress)

ception, namely to read or interpret trees from “left to right” and

to conclude that there is an element of progress from left to right

when there is not (the so-called “primitive lineage fallacy”, Omland

et al. 2008). All branches can be freely rotated around the nodes

without changing the topology or any other information content of

platypus kangaroo human mouse deer aardvarkanteater

the tree. Consequently, all three trees in Fig. 1 are actually exactly

the same tree, although we are clearly more used to seeing ver-

sion A than B or C. Interpreting trees as ladders of progress also

introduces another linguistic mistake: taxa do not branch off the

tree. This would imply a main trunk, i.e. a main direction of the tree

(as in the famous Tree of Life by Ernst Haeckel). Such a main trunk,

however, does not exist; all possible trajectories from the root of the

tree to any of its tips are equivalent! There is only branching (into

sister groups), no branching off. In the words of Omland et al. (2008, 2

p. 863): “Stating which is the lineage to ‘branch off’ requires a ﬁxed

reference that deﬁnes where evolution is heading” – clearly a long-

outdated view of evolution as a predetermined (“orthogenetic”)

process.

As a consequence, no terminal taxon in a phylogenetic tree

(cladogram, phylogram, chronogram) can be basal (basal to what

anyway? It is just as “far away” from its ancestor as its sister

group). Basal taxa exist, but not at the tips of trees, they are inter-

nal ancestral or stem species (see circles 1 and 2 in Fig. 1). The

mouse hu nam deer anteater aardvark k na g ra o lpo pyta su

ﬁrst split in Fig. 1 is indeed more basal (older) than split 2, but

apart from this speciﬁc context there is no use for the term basal

when describing a tree. Nor can taxa as a whole be primitive,

plesiomorphic, advanced, progressive or apomorphic; these terms

apply to characters and their various states – species and other

taxa are always an amalgam of plesiomorphies and apomorphies.

The platypus, sometimes viewed as the archetypically primitive

mammal (after all, it lays eggs) is in point of fact highly derived

with respect to a number of characters (the bill with its electrore-

ception and the venom spur, to name just the two most obvious

ones) (see Omland et al. 2008 for a web search of the platypus as

being primitive). With the possible exception of surviving stem

species (a highly contentious issue in phylogenetics), no extant

taxon can be ancestral to another. As Omland et al. (2008) rightly

state, phylogenies of extant (perhaps better: terminal) species

“show ‘evolutionary cousin’ relationships and should not imply Fig. 1. Three equivalent depictions of the same phylogenetic tree of representatives

of major mammalian taxa: Monotremata (platypus), Marsupialia (kangaroo), and

one species is more primitive, whereas another is more advanced”

different groups within the Placentalia (Xenarthra: anteater, Afrotheria: aardvark,

(p. 856; they illustrate this with a pedigree of the Kennedy fam-

Laurasiatheria: deer, Euarchontoglires: mouse and human). Whether xenarthrans

ily).

and afrotherians are really sister taxa is still being debated, but this is irrelevant

Still, the evolutionary and phylogenetic literature teems with for the present purpose. Version A shows the traditional way of representation

these biologically incorrect expressions. Omland et al. (2008) with monotremes on the far left, followed by marsupials and placental mammals.

Humans are usually shown on the far right, implying a “ladder of progress” from

give examples of which mammal species they found to be

“primitive” monotremes and “slightly less primitive” marsupials to more “derived”

called primitive (expectedly, the opossum, monotremes, shrews

placental mammals with humans at the top. This, however, is not implied in any of

and tenrecs ranked ﬁrst). And consider this quote from the

the three trees, nor is it (bio-)logically correct. Only the y-axis, but not the x-axis,

English Wikipedia site on mammals (https://en.wikipedia.org/ carries directional information (time). The circles with numbers 1 and 2 denote

the ﬁrst (and indeed most basal) split in the tree, i.e. the stem species giving rise

wiki/Mammal, accessed on 4 October 2015, italics added): “The

to monotremes and therians, and the second (less basal) split of the therian stem

relationships between these three lineages is contentious, and

species giving rise to marsupials and placental mammals.

three different hypotheses have been proposed with respect to

which group is basal with respect to other placentals. These

Editorial / Mammalian Biology 81 (2016) 185–188 187

hypotheses are Atlantogenata (basal Boreoeutheria), Epitheria Practical guidelines for phylogenetic and taxonomic papers

(basal Xenarthra), and Exafroplacentalia (basal Afrotheria).” The in Mammalian Biology

whole entry “Basal (phylogenetics)” (https://en.wikipedia.org/

•

wiki/Basal (phylogenetics), accessed on 5 October 2015) is even Do not present phylogenetic trees as “ladders of progress”! In par-

more revealing, betraying serious misconceptions of phyloge- ticular, refrain from using terms like “higher” and “lower” when

netic theory. The only directional information in trees is along referring to taxa.

•

the time axis and along various character state trajectories Avoid language that treats phylogenetic trees as having a “main

from plesiomorphic to apomorphic (if these states are plotted trunk” – trees are just successions of branching events, and in

on the tree), but the latter will form different zigzag lines in each such event two equivalent sister lineages arise. There is no

the tree due to mosaic evolution rather than a single straight direction, nor is any of the two sister lineages more basal or more

line. advanced, primitive or progressive, etc. than the other! In other

The reason that the “primitive lineage fallacy” and reading words: there is branching, but no branching “off” of any alleged

trees as ladders of progress is so widespread is almost certainly main trunk of a phylogenetic tree.

•

a relic of a concept once popular among natural philosophers, Do not treat any terminal taxon as ancestral to another.

•

the scala naturae or “great chain of being” (Lovejoy 1936), the The terms plesiomorphic and apomorphic as well as related

idea that everything that exists can be arranged in a hierarchi- expressions (primitive, derived, advanced, etc.) are applicable

cal scheme from lowest (inanimate objects) through all kinds of only to characters/character states, not to taxa. Taxa always

living beings to highest (God). Needless to say, humans rank high- combine plesiomorphic and apomorphic traits (except for

est among the earthly living beings. Language making reference hypothetical stem species which, by deﬁnition, lack exclusive

(probably often unconsciously) to this concept (terms like higher apomorphies).

•

and lower, basal, primitive, etc.) permeates the evolutionary lit- When describing and/or splitting species make explicit refer-

erature (see above and Rigato and Minelli 2013). While there is ence to the species concept you are basing your decision on and

of course increasing complexity in many lineages (just as there explain (based on your data) why you consider the level of

is decreasing complexity), progress is an illusion of the human distinctness sufﬁcient for taxonomic recognition at the species

mind! More than 150 years after the Origin of Species it is, at level.

•

long last, time to abandon these pre-evolutionary notions and Species are such fundamental and important units that they

purge our scientiﬁc language from any terminology perpetuating should not be introduced carelessly. Species description and

them. splitting based on superﬁcial data like simple morphometric

differences (including those that are statistically signiﬁcant),

arbitrary values of genetic distance or phylogenetic relation-

Species splitting and the description of new species ships derived from limited molecular datasets (single-locus

analyses, particularly mtDNA) is strongly discouraged. All

Species delimitation, particularly the splitting of one into two or of these may serve to support conclusions derived from

more species and the (often) underlying notion of the diagnosabil- more appropriate datasets, but are not sufﬁcient on their

ity version of the Phylogenetic Species Concept (dPSC), has recently own.

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been a much debated topic in mammalian taxonomy (see refer- In the case of allopatric populations, divergence (e.g. genetic dis-

ences above; Zachos in press presents a synthesis and extensive tance) similar to that known from sympatric sister species is not in

discussion). Apart from theoretical arguments, conservation corol- itself an argument for separate species as it erroneously assumes

laries (epitomized by the title “The species and the specious” of a identical evolutionary processes in sympatry and allopatry (see,

comment in Nature on the occasion of the tercentenary of Linnaeus, for example, Zachos in press and references therein).

Marris 2007) have also been discussed at length, naturally with dif-

fering conclusions (e.g. Agapow et al. 2004; Frankham et al. 2012;

Gippoliti and Groves 2012; Zachos et al. 2013b). The situation with References

species delimitation is much more complex than the interpreta-

Agapow, P.-M., Bininda-Emonds, O.R.P., Crandall, K.A., Gittleman, J.L., Mace, G.M.,

tion of phylogenetic trees, mostly because reading trees as ladders

Marshall, J.C., Purvis, A., 2004. The impact of species concept on biodiversity

of progress is simply wrong, whereas species delimitation is much

studies. Q. Rev. Biol. 79, 161–179.

more of a grey area. Because all 27 or so species concepts are based Baum, D.A., Smith, S.D., Donovan, S.S.S., 2005. The tree-thinking challenge. Science

310, 979–980.

on biological realities (such as interfertility, diagnosability, mono-

Cotterill, F.P.D., Taylor, P.J., Gippoliti, S., Bishop, J.M., Groves, C.P., 2014. Why one

phyly, genetic compatibility and isolation, ecological niches and

century of phenetics is enough: response to ‘Are there really twice as many

many more), none of them can be wrong in a logical way (Zachos in bovid species as we thought?’. Syst. Biol. 63, 819–832.

Frankham, R., Ballou, J.D., Dudash, M.R., Eldridge, M.D.B., Fenster, C.B., Lacy, R.C.,

press). It is much more a question of whether they are appropriate,

Mendelson III, J.R., Porton, I.J., Ralls, K., Ryder, O.A., 2012. Implications of different

feasible and consistent, which of course leaves much more room

species concepts for conserving biodiversity. Biol. Conserv. 153, 25–31.

for subjective opinion and interpretation. Ultimately, all species Gippoliti, S., Groves, C.P., 2012. “Taxonomic inﬂation” in the historical context of

mammalogy and conservation. Hystrix It. J. Mammal. 23, 6–9.

concepts denote population lineages at some level or other in the

Groves, C.P., 2013. The nature of species: a rejoinder to Zachos et al. Mammal. Biol.,

Tree of Life, which is why the Evolutionary Species Concept or 7–9.

related deﬁnitions are often viewed as the primary species con- Heller, R., Frandsen, P., Lorenzen, E.D., Siegismund, H.R., 2013. Are there really twice

as many bovid species as we thought? Syst. Biol. 62, 490–493.

cept, whereas all the other so-called species concepts are rather

Heller, R., Frandsen, P., Lorenzen, E.D., Siegismund, H.R., 2014. Is diagnosability an

secondary species identiﬁcation criteria. I will not go into further

indicator of speciation? Response to “Why one century of phenetics is enough”.

detail here, but refer the readers to the literature cited and refer- Syst. Biol. 63, 833–837.

ences therein. Isaac, J.B., Mallet, J., Mace, G.M., 2004. Taxonomic inﬂation: its inﬂuence on macroe-

cology and conservation. Trends Ecol. Evol. 19, 464–469.

Against this background, introducing precise rules on when to

Krell, F.-T., Cranston, P.S., 2004. Which side of the tree is more basal? Syst. Entomol.

allow species splitting and/or the description of a new species

29, 279–281.

would border on editorial censorship. The guidelines below in as Lovejoy, A.O., 1936. The Great Chain of Being: A Study of the History of an Idea.

Harvard University Press, Cambridge, MA.

far as they pertain to taxonomy should therefore rather be viewed

Marris, E., 2007. The species and the specious. Nature 446, 250–253.

as recommendations, but serious ones as species splitting will be

Omland, K.E., Cook, L.G., Crisp, M.D., 2008. Tree thinking for all biology: the problem

subjected to close scrutiny by both referees and editors. with reading phylogenies as ladders of progress. BioEssays 30, 854–867.

188 Editorial / Mammalian Biology 81 (2016) 185–188

Rigato, E., Minelli, A., 2013. The great chain of being is still there. Evol. Educ. Outreach Zachos, F.E., Apollonio, M., Bärmann, E.V., Festa-Bianchet, M., Göhlich, U., Habel, J.C.,

6, 18. Haring, E., Kruckenhauser, L., Lovari, S., McDevitt, A.D., Pertoldi, C., Rössner, G.E.,

Zachos, F.E., 2015. Taxonomic inﬂation, the Phylogenetic Species Concept and lin- Sánchez-Villagra, M.R., Scandura, M., Suchentrunk, F., 2013a. Species inﬂation

eages in the Tree of Life – a cautionary comment on species splitting. J. Zool. and taxonomic artefacts — a critical comment on recent trends in mammalian

Syst. Evol. Res. 53, 180–184. classiﬁcation. Mammal. Biol. 78, 1–6.

Zachos, F.E., 2015. Species concepts and species delimitation in mammals. In: Zachos, Zachos, F.E., Clutton-Brock, T.H., Festa-Bianchet, M., Lovari, S., Macdonald, D.W.,

F.E., Asher, R. (Eds.), Mammalian Evolution, Diversity and Systematics. Hand- Schaller, G.B., 2013b. Species splitting puts conservation at risk. Nature 494,

book of Zoology, Mammalia Series. De Gruyter, Berlin, ISBN 978-3-11-027590-2 35.

(in press).