[Paleopsych] Robert O'Hara: Population Thinking and Tree Thinking in Systematics

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Population Thinking and Tree Thinking in Systematics

    This is a web version of a previously published paper that was first
    presented at the Royal Swedish Academy of Sciences in Stockholm as
    part of a symposium honoring the 25th anniversary of the journal
    Zoologica Scripta. A version of this paper in portable document
    format, suitable for printing, is [10]also available. In the web
    version the text is reproduced in its entirety but no figures are
    included. Editorial insertions in the web version are enclosed in
    [INS: {braces} :INS] . Citations to this paper should refer to the
    original printed version:

    O'Hara, Robert J. 1997.
    Population thinking and tree thinking in systematics. Zoologica
    Scripta, 26(4): 323-329.

Population Thinking and Tree Thinking in Systematics

     Robert J. O'Hara
     Cornelia Strong College and Department of Biology
     University of North Carolina at Greensboro
     Greensboro, North Carolina 27402 U.S.A.


    Two new modes of thinking have spread through systematics in the
    twentieth century. Both have deep historical roots, but they have been
    widely accepted only during this century. Population thinking overtook
    the field in the early part of the century, culminating in the full
    development of population systematics in the 1930s and 1940s, and the
    subsequent growth of the entire field of population biology.
    Population thinking rejects the idea that each species has a natural
    type (as the earlier essentialist view had assumed), and instead sees
    every species as a varying population of interbreeding individuals.
    Tree thinking has spread through the field since the 1960s with the
    development of phylogenetic systematics. Tree thinking recognizes that
    species are not independent replicates within a class (as earlier
    group thinkers had tended to see them), but are instead interconnected
    parts of an evolutionary tree. It lays emphasis on the explanation of
    evolutionary events in the context of a tree, rather than on the
    states exhibited by collections of species, and it sees evolutionary
    history as a story of divergence rather than a story of development.
    Just as population thinking gave rise to the new field of population
    biology, so tree thinking is giving rise to the new field of
    phylogenetic biology.


    The history of systematics in the twentieth century can be broadly
    divided into two periods. The first is the period of population
    systematics, which began at the turn of the century and flourished
    especially through the years of the Modern Synthesis of the 1930s and
    1940s and beyond (Mayr & Provine 1980). The second period is the
    period of phylogenetic systematics which began during the 1960s and
    which continues to flourish today (de Queiroz 1997).

    During the period of population systematics much of the work of the
    systematics community was directed toward studies of geographical
    variation, speciation, and microevolutionary processes, and a great
    many practical and theoretical advances were made in all of these
    areas. The theory of allopatric speciation was comprehensively
    developed, especially for vertebrates; large series of specimens for
    the study of geographical variation were assembled in museums; the
    application of statistical techniques became widespread; and studies
    of cytological and biochemical variation began to be added to
    traditional studies of gross anatomical variation.

    The period of phylogenetic systematics, beginning in the 1960s, has
    seen a shift in emphasis toward larger questions of evolutionary
    history and the structure of the evolutionary tree, and, just as in
    the earlier period, this newer phylogenetic era has seen and continues
    to see many advances in systematic theory and practice. The
    development of all the tools and concepts of cladistic analysis has
    been the most important advance of this period; the distinction
    between ancestral and derived character states; the application of
    computational techniques for reconstructing trees; the increasing
    availability of data on molecular anatomy to supplement the data of
    gross anatomy; and more recently the application of phylogenetic
    information to problems in many other biological fields from ecology
    to physiology to embryology to behavior.

    The distinction between the two periods of population systematics and
    phylogenetic systematics is not sharp, of course, and there continues
    to be much fine work done today in population systematics, just as
    there were important contributions to the study of phylogeny before
    the 1960s. But the general distinction between these two periods is
    real, and it captures a variety of important practical, theoretical,
    and disciplinary developments in the history of twentieth-century

    At the broadest level, beyond the development of particular techniques
    or concepts, each of these two periods may be characterized by the
    introduction and spread of new ways of thinking about systematic and
    evolutionary problems, ways of thinking that correspond in scope to
    the scientific "themata" described by Holton (1973) for the physical
    sciences. Distinctive of the period of population systematics was the
    spread of what is commonly called "population thinking" (Mayr, 1959,
    1975), and distinctive of the period of phylogenetic systematics has
    been the spread of what may be called "tree thinking" (O'Hara, 1988).
    My aim here is to outline the components of tree thinking, as a way of
    undertanding some of the larger changes that have taken place since
    the 1960s. Before we consider tree thinking, however, let us look at
    the idea of population thinking by way of comparison.

Population thinking

    The term "population thinking" was coined by Ernst Mayr in 1959. In
    coining the term Mayr did not claim to be describing something new;
    rather he intended to capture with the term a way of thinking that had
    swept through systematics and evolutionary biology generally in the
    first half of the twentieth century. (Mayr in fact traces the idea of
    population thinking back to the early 1800s, but I think it is fair to
    say that its hold within systematics did not become widespread until
    early in the twentieth century.)

    To understand the idea of population thinking it is necessary to
    contrast it with the mode of thought it replaced, which Mayr calls
    typology or essentialism. In simple terms, an essentialist sees
    individual variation within a species as error. An essentialist would
    in no way deny the existence of individual variation; it obviously
    does exist. But for an essentialist every species has a natural form,
    a true type, and individual variation within that species represents
    accidental deviation from that true type caused by external
    environmental influences. In the absence of external influences that
    cause individuals to deviate from their true type all individuals of a
    species would be forever the same, because each species' type remains
    fixed through time.

    The French naturalist Buffon expressed the essentialist view well in
    his Histoire Naturelle in 1753 (Sloan 1987: 121):

      There is, in nature, a general prototype in each species upon which
      each individual is modeled, but which seems, in realizing itself,
      to be altered or perfected by circumstances. So that, relative to
      certain characteristics, there is an unusual variation in the
      appearance in the succession of individuals, and at the same time a
      constancy in the species as a whole which appears remarkable. The
      first animal, the first horse, for example, has been the external
      model and the internal mold upon which all horses which have ever
      been born, all those which now exist, and all which will arise,
      have been formed. But this model, which we know only by its copies,
      has been able to be altered or perfected in the communication and
      multiplication of its form. The original impression subsists in its
      entirety in each individual, but although there might be millions
      of them, none of these individuals is similar in entirety to any
      other, nor, by implication, to the impressing model.

    Elliott Sober (1980, 1994) has provided a very thorough examination of
    the idea of essentialism as it applies to species, drawing on what he
    calls the "natural state model" of Aristotle, and I recommend his work
    to all who are interested in this subject. Sober's discussion can be
    fruitfully compared with those of Toulmin (1961) and Kuhn (1977) on
    the conceptual framework of early chemistry and physics.

    In contrast to the essentialist, the population thinker rejects
    entirely the idea that species have "types" or "natural states."
    Individual variation within a species is not deviation from a natural
    state under the influence of external forces, a natural state to which
    the species will return if the forces are removed. Rather, the range
    of individual variation within a species is the result of ongoing
    processes of mutation and recombination, the production of phenotypes
    in the available environments, and then the selection of those
    phenotypes from generation to generation. Nothing remains invariant
    across time because new individuals are not produced from some
    permanent "internal mold," but instead are produced directly from
    their parents, and they incorporate new heritable variations in each
    generation. This allows species to "depart indefinitely" (Wallace
    1858) from their ancestors, and in so doing it dissolves the idea of
    an enduring species type altogether.

    In passing it is worthwhile to note that even though population
    thinking has by now thoroughly permeated systematics and evolutionary
    biology generally, there are other biological fields, most notably
    medicine, where it has made little headway. Medical notions of health
    and disease have strong essentialist overtones, and as medicine has
    come to focus more on the genetic traits of individuals (as opposed to
    external agents of infection) there is a tendency on the part of
    medical practicioners to pathologize normal variation in human
    populations, and in so doing to resurrect the idea of a "natural type"
    for Homo sapiens, an idea long ago rejected by evolutionary biology.

Tree Thinking

    If the spread of population thinking characterized the period of
    population systematics, then the spread of what we may call "tree
    thinking" (O'Hara 1988; Maddison & Maddison 1989; de Queiroz 1992;
    Doyle & Donoghue 1993; Wake 1994) has characterised the period of
    phylogenetic systematics. Tree thinking is in no sense a successor to
    population thinking, which is just as important today as it has ever
    been. Tree thinking is simply the phylogenetic counterpart to
    population thinking, and like population thinking it has brought a
    more completely evolutionary perspective to systematics (de Queiroz
    1988, 1992, 1997; O'Hara 1988, 1992, 1996).

    What constitutes tree thinking, and more especially what constitutes
    the absence of tree thinking? If population thinking is contrasted
    with essentialism, then with what should we contrast tree thinking?

    Tree thinking may be contrasted with two other ways of thinking about
    systematics and large-scale evolutionary phenomena. The first of these
    I call "group thinking," and the second I call "developmental
    thinking." Let us consider each in turn, and consider how tree
    thinking differs from them.

    Group thinking has been a long-standing way of thinking in
    systematics, and group thinking equates "systematics" with
    "classification." Just as we can classify many kinds of
    objects--landforms, books, minerals, stars--so in the same way can we
    classify species, says the group thinker. Group thinking in
    systematics (and classificatory thinking in general) treats each
    member of a particular group as an independent replicate, and this is
    key. Each neutron star, for example, is an instance of the class of
    neutron stars, an independant replicate that can teach us something
    about the nature of neutron stars as a class. Each drumlin is an
    independent replicate of the landform group "drumlins" and can give us
    insight into the common causes of drumlins--the common processes
    responsible for the formation of all drumlins. The goal is to abstract
    from the replicate instances a general picture that will describe all
    members of the class and account for their existence.

    Group thinking of this kind--seeing members of a group as replicate
    instances--is quite appropriate for many kinds of scientific inquiry,
    such as the study of stars or landforms, but it breaks down when we
    try to apply it to species. It breaks down for the fundamental reason
    that species are not independent replicates: they are parts of a
    connected tree of ancestry and descent, and they inherit most of their
    attributes in a way that stars and landforms, for example, do not.

    Tree thinking, in contrast to group thinking, considers species in a
    phylogenetic context, not as independent replicates but as parts of a
    single phylogenetic tree. If we seek to understand common causes
    acting in evolution then the replicates we need to examine are not
    species, but the evolutionary events that are of interest in a
    particular study, and this can only be done by plotting those events
    on a tree. If we are interested in why ten species in a larger group
    exhibit a particular trait (say a trait that is correlated with the
    occupation of a certain environment) then we must first ask, in the
    context of a tree, whether this situation represents ten independent
    originations of the trait, or eight with two subsequent speciations,
    or five, or three, or perhaps only one independent origination event
    with the ten separate species all retaining the trait through
    inheritance. These questions can only be answered in the context of a

    The focus on explaining evolutionary events rather than the states of
    supposedly replicate species, and on determing where the events occur
    on a phylogeny, is central to tree thinking. This new phylogenetic
    orientation has in recent years opened the door to a whole range of
    important studies of adaptation, ecology, physiology, and other areas
    that long been approached from ahistorical, synchronic perspectives
    (Fink 1982; Lauder 1982; Felsenstein 1985; Huey 1987; Coddington 1988;
    Ronquist & Nylin 1990; Wanntorp et al. 1990; Brooks & McLennan 1991;
    Harvey & Pagel 1991; Vane-Wright et al. 1991; Stiassny 1992).

    Although tree thinking as I have described it is an aspect of
    systematic biology, the idea of tree thinking isn't necessarily tied
    to living things--all it requires is descent and inheritance. A
    fascinating inorganic example of tree thinking can be found in a
    recent paper on the motion of asteroids (Milani & Farinella 1994), an
    example which makes use of many of the same ideas I have just
    outlined. In examining the orbits of asteriods it is often possible to
    identify groups of asteroids that have motion characteristics in
    common. One might be tempted to assume that there is something about
    the composition of this group of asteroids or about their location
    that causes this common "phenotype" (if you will) to exist. But Milani
    and Farinella have shown that these asteroids do not share certain
    characteristics of motion because of some common set of external
    forces acting on them; they share common patterns of motion because
    they literally inherited that motion from an ancestral asteroid of
    which they once were parts and which subsequently broke up into the
    pieces we now see. The asteroids in this group are not independent
    replicates that constitute a class, but rather are parts of a tree of
    inheritance and their common characteristics can be explained by
    reference to their shared history.

    There is another aspect of group thinking that tree thinking is
    supplanting, and that is the traditional inclination to regard taxa of
    equal rank within certain large groups as equivalent and comparable in
    some sense. (This is a higher level version of the
    species-as-replicates perspective.) An example concerns the
    traditional orders of birds, the largest of which is the Passeriformes
    which by itself contains about half of all bird species, with the
    other 30 or so traditional orders containing all the rest. The
    ornithologist Robert Raikow wrote a paper called "Why are there so
    many kinds of passerine birds?" (1986) in which he argued in part that
    this question is misplaced because it assumes that the various
    "orders" of birds are in some way comparable groups when in fact they
    are not. And further, even if we frame a more precise comparison
    between the Passeriformes and their sister clade, and ask why each of
    these two groups differs in species richness, here the validity of the
    question will depend upon the internal structure of the passeriform
    tree (Fig. 1). Framing these questions in the context of a tree is
    essential if progress is to be made, a point that some of Raikow's
    commentators did not appear to fully grasp (Raikow 1988).

    Let us now turn from group thinking as contrasted with tree thinking,
    to what may be called "developmental thinking" and contrast this also
    with tree thinking.

    By "developmental thinking" I mean thinking that sees evolutionary
    history as a story of individual development or unfolding--a story of
    "evolution" in the original sense of the word. There is a
    long-standing tradition in evolutionary writing of describing the
    course of evolution as a developmental course running from monad to
    man. This tradition pre-dates evolution certainly; the evolutionary
    version is really a temporalization of the ancient idea of the Chain
    of Being (Lovejoy 1936).

    Evolutionary histories of the developmental type don't narrate a
    tree--a branching history--they select one important endpoint (usually
    us) and then trace up from the root through the tree to that endpoint,
    employing a variety of narrative and nomenclatural devices that
    minimize the branching aspect of evolution. In other papers (O'Hara
    1988, 1992, 1993) I have discussed in detail the narrative and
    graphical devices that have traditionally been used to minimize the
    branching aspect of evolutionary history and to thereby create a
    linear, developmental aspect.

    Tree thinking, in contrast to this sort of developmental thinking,
    emphasizes the divergent character of evolutionary history and the
    complexity and irregularity of the evolutionary tree. I'm afraid to
    say, however, that while many contemporary systematists no longer
    think of evolution as a developmental story and no longer draw
    diagrams that show humans as the pinnacle of life, most of the general
    public and most of our students still do. A survey of beginning
    biology students' understanding of evolutionary history almost
    invariably produces images of the developmental type with a long main
    line reaching to vertebrates, mammals, or humans (Fig. 2). One of the
    main objectives of the systematics community for the next decade
    should be the preparation of educational materials for beginning
    students to teach them to become tree thinkers (O'Hara 1994). Just as
    beginning students in geography need to be taught how to read maps, so
    beginning students in biology should be taught how to read trees and
    to understand what trees communicate (Figs. 3, 4). One effective
    method of jarring students out of the traditional pattern of
    developmental thinking is to show them trees that are purposely drawn
    from a different evolutionary perspective (Fig. 5), although few such
    trees are now available.

Systematics and palaetiology

    When William Whewell, the nineteenth-century polymath, compiled his
    comprehensive survey of all the sciences (Whewell 1847), he placed
    systematic zoology and systematic botany along with mineralogy in the
    category "classificatory sciences." Elsewhere in his survey, however,
    Whewell created a new class of sciences which he called by the awkward
    name "palaetiological sciences"--the sciences of history and
    historical causation. Into this new category Whewell put such
    seemingly disparate fields as geology and comparative philology,
    fields he saw as united by their common aim of historical
    reconstruction (O'Hara 1996). Charles Lyell's geological work, which
    was new at the time, helped to shape Whewell's characterization of the
    palaetiological sciences. When Charles Darwin began to work seriously
    on the species question he didn't take as his model the approaches of
    the classificatory sciences; he took as his model the palaetiological
    science of Lyell. Indeed, the Origin of Species is almost a casebook
    of the palaetiological principles that Whewell had outlined. Darwin in
    effect took systematic biology out of the classificatory sciences and
    placed it squarely among the palaetiological sciences, and in so doing
    he set for us a range of historical problems the full implications of
    which are still being discovered today (de Queiroz 1988; O'Hara 1988,
    1992, 1993; de Queiroz & Gauthier 1992, 1994; Williams 1992).

    "As buds give rise by growth to fresh buds," wrote Darwin in one of
    his more literary passages (1859: 130), "and these, if vigorous,
    branch out and overtop on all sides many a feebler branch, so by
    generation I believe it has been with the great Tree of Life, which
    fills with its dead and broken branches the crust of the earth, and
    covers the surface with its ever branching and beautiful
    ramifications." The tree of life has proven to be a subtle construct,
    more subtle perhaps than Darwin suspected. But the spread of tree
    thinking throughout systematics in the last thirty years, and its more
    recent spread from systematics to other fields, has brought a new
    clarity to our understanding of the tree of life, an idea that is
    fundamental to all of evolutionary biology.


    I am grateful to Per Sundberg, Marit Christiansen, and Fredrik Pleijel
    of Zoologica Scripta, as well as to the Norwegian Academy of Science
    and Letters and the Royal Swedish Academy of Sciences for their kind
    invitation to participate in this anniversary symposium. Margareta
    Wilberg handled all the arrangements expertly, and Per Sundberg
    extended especially kind hospitality during my stay in Sweden. Jeremy
    Ahouse directed my attention to Scott's tree of butterfly evolution.
    Gregory Mayer, Kevin de Queiroz, and Fredrik Pleijel offered valuable
    comments on the manuscript.


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[INS: {Figure Captions} :INS]

    Fig. 1. -- Two sister taxa differing in species richness (A). One
    might be inclined to assume that the speciose taxon possesses a "key
    innovation" that has caused it to speciate at a greater rate than its
    sister taxon. Such an assumption may or may not be warranted depending
    upon the internal structure of the speciose clade. If the internal
    structure is as shown in (B) then it is unlikely that clade B
    possesses any special innovation, although its sub-clade B' may.

    Fig. 2. -- An evolutionary tree drawn by an undergraduate biology
    student at the University of Wisconsin--Madison. At the beginning of a
    course each student was asked to "sketch an evolutionary tree of life,
    and label as many branches as you can. Don't worry if your tree is not
    perfect or if you can't remember technical terminology; this is not a
    graded exercise, and you should not even put your name on the page."
    Most trees the students produced have as their longest branches the
    ones leading humans or to mammals or vertebrates generally.

    Fig. 3. -- A phylogeny of three taxa shown in four different graphical
    styles (A-D), from O'Hara (1994: 14). All four of these diagrams
    convey exactly the same information about the three taxa.
    Non-specialists and beginning biology students need to be taught to
    read modern evolutionary trees just as beginning students of geography
    need to be taught to read maps.

    Fig. 4. -- A phylogeny of eight taxa (A), and two simplified versions
    of that phylogeny (B-C), from O'Hara (1994: 14). If students and
    non-specialists are to become tree thinkers they must learn to
    recognize how trees can be differentially simplified (or
    differentially resolved) to show the details of particular branches.

    Fig. 5. -- "The evolutionary tree of animals, especially those along
    the line that evolved into butterflies," from Scott (1986: 87).
    Vertebrates appear on the lower left. Trees such as this can jar
    students and non-specialists into thinking about the assumptions
    behind traditional human-centered trees such as the one shown in Fig.
    2. Numbers on this tree represent millions of years.


    3. http://rjohara.net/cv/publications.html
    5. http://rjohara.net/accesskeys/
    7. http://rjohara.net/search/
    8. http://rjohara.net/cv/
   10. http://rjohara.net/cv/1997Scripta.pdf
   11. http://rjohara.net/cv/1988SZ.html
   12. http://rjohara.net/cv/1992BP.html
   13. http://rjohara.net/cv/1993SB.html
   14. http://rjohara.net/cv/1994AZ.html
   15. http://rjohara.net/cv/1996Milan.html
   16. http://rjohara.net/

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