- Email: [email protected]
Species concepts versus species criteria
News & Comment
TRENDS in Parasitology Vol.18 No.10 October 2002
439
most appealing, it is essential to provide the necessary foundations. Although I appreciate that space limits could have prevented a more detailed discussion on this vast subject, with a little additional material, readers can be provided with a more complete picture and a more accessible bibliography. To provide readers with at least some context in this subject, it is therefore useful to consider the development of species thinking, particularly since the blossoming of evolutionary theory. Pre-darwinian approaches to species were based on Aristotle’s notion of ‘ideal’, where organisms have a natural state, and variation between organisms reflected the imperfection of nature. Such essentialist thinking defined species by individual characteristics that were both necessary and sufficient (i.e. species were considered as discrete units, where all members share a set of characters). Interestingly Aristotle’s concept on what characterizes an organism’s natural state was based on reproduction: fidelity of reproduction is a natural state of an organism. Such a discrete nature of a species, however, conflicts with darwinian theory, where evolution is considered a continuous process. Mayr’s biological species concept (BSC) offered an alternative to such essentialist thinking [9]. Although Mayr’s biological universal was also based on reproductive potential, it has one implicit but often unstated difference. What Mayr actually achieved was majestic; as an alternative to the individual-based approach, Mayr developed on a population-based approach. Evolutionary theory concerns itself with the properties of populations and the result of historical action on those properties. Rather than attempting to explain observed population phenomena by examining the characters of individual organisms, population thinking considers such phenomena as legitimate in their own right without trying to reduce them to the collective consequences of the individual (see Ref. [8]). By this, Mayr circumvented the problem inherent in the organismal level approach, wherein the criteria that specify when an organism belongs to a species instantly defines a group in terms of an individual property. The problem is what if local variation in a population confounds the criteria, even though the population
still belongs to the species (i.e. how to define the species in spite of natural variation?). Population thinking offered an alternative to such reductionism and brought species thinking in line with evolutionary theory. Since Mayr, there has been considerable debate and many developments in species thinking. As Kunz has pointed out, BSC excludes certain organisms (e.g. those reproducing clonally) and is often difficult to assess in many situations [1]. Incidentally, Kunz is incorrect in highlighting island populations as being automatically excluded from definition by BSC because Mayr stated ‘actually or potentially interbreeding populations’. On a final note, although it is now generally agreed that species are segments of population-level evolutionary lineages, there remains some debate over the value of having a species definition when aiming to understand the speciation process [10,11]. Understanding speciation and being able to define what constitutes a species is of paramount importance to parasitologists, especially those working in medical and veterinary parasitology. Certainly, species criteria could be different across parasitic taxa, but the extensive parasitological knowledge should enable parasitologists to make a valuable contribution to the species and speciation debate, as well as establishing practical criteria for pathogenic species identification.
Letters
Species concepts versus species criteria It was initially with great pleasure that I read the recent article of Werner Kunz addressing the issue of species, with respect to parasites [1]. However, despite a good introduction to this domain, this article side steps a rigorous analysis of the species problem: what is a species? This may not be surprising because it has been one of the most vexing issues in biology for decades. Kunz addresses all the relevant components of the species issue, discussing the problems of species diagnosis by using traits, the biospecies concept based on the capacity (trait) to interbreed, and goes as far as to introduce cladistics and classification according to evolutionary lineages. However, Kunz fails to resolve the important difference between concepts and criteria, which lies at the heart of the issue. Indeed, a recent discussion of this topic clearly indicates where the confusion lies [2,3]: there has been a tendency to confuse species concepts (ideas on the kind of entity that is designated a species category) and species criteria (the standard for judging whether an entity qualifies as a member of a species category). The species criteria provides a list on which to judge if groups of individuals are distinct species (e.g. there are intrinsic barriers to genetic exchange, species are diagnosable by fixed character states). The species concept should be concerned with defining a species according to some biological universal [4]. Although there have been a dozen or so suggested species concepts, all modern versions, including the cited Cracraft (1983) [5], are actually variations on a common theme of what designates a species – a group (population) of organisms occurring at a cross-section in an evolutionary lineage (where lineage is a single line of direct ancestry and descent). This idea was originally outlined by Ghiselin [6] and Hull [7]: organisms are conspecific by virtue of their actual historical relationships to each other and not according to their genotypic or phenotypic similarity (i.e. species are chunks of phylogenetic nexus [8], not natural kinds). If, as Kunz suggests, we are to encourage parasitologists into the species debate and the study of speciation, an idea that I find http://parasites.trends.com
Richard Paul Unité de Biochimie et Biologie Moléculaire des Insectes, Institut Pasteur, 28 rue du Dr. Roux, 75724 Paris cedex 15, France. e-mail: [email protected] References 1 Kunz, W. (2002) When is a parasite species a species? Trends Parasitol. 18, 121–124 2 de Queiroz, K. (1998) The general lineage concept of species, species criteria, and the process of speciation: a conceptual unification and terminological recommendations. In Endless Forms: Species and Speciation (Howard, D.J. and Belocher, S.H. eds), pp. 57–75, Oxford University Press 3 Harrison, R.G. (1998) Linking evolutionary pattern and process: the relevance of species concepts for the study of speciation. In Endless Forms: Species and Speciation (Howard, D.J. and Belocher, S.H. eds), pp. 19–31, Oxford University Press 4 Templeton, A.R. (1998) Species and speciation: geography, population structure, ecology, and gene trees. In Endless Forms: Species and Speciation (Howard, D.J. and Belocher, S.H. eds), pp. 32–43, Oxford University Press
1471-4922/02/$ – see front matter © 2002 Elsevier Science Ltd. All rights reserved. PII: S1471-4922(02)02319-X
440
News & Comment
5 Cracraft, J. (1983) Species concepts and speciation analysis. Curr. Ornithol. 1, 159–187 6 Ghiselin, M. (1974) A radical solution to the species problem. System. Zool. 23, 536–544 7 Hull, D. (1976) Are species really individuals? System. Zool. 25, 174–191 8 Sober, E. (1984) The Nature of Selection: Evolutionary Theory in Philosophical Focus, Massachusetts Institute of Technology Press 9 Mayr, E. (1963) Animal Species and Evolution, Belknap Press 10 Templeton, A.R. (1989) The meaning of species and speciation: a genetic perspective. In Speciation and its consequences (Otte, D. and Endler, J.A. eds), pp. 3–27, Sinauer 11 Bush, G.L. (1994) Sympatric speciation in animals: new wine in old bottles. Trends Ecol. Evol. 9, 285–288
Published online: 21 August 2002
Species concepts versus species criteria Response from Werner Kunz
Richard Paul’s letter is of great importance for parasitologists because it highlights the species debate. Within a group of similar parasitic individuals, some can be specific for one host, others for another; some can be pathogenic, others not; some can be sensitive to a drug and others are resistant. As a result of these data, individual parasites can be classified into groups. In several cases, host specificity, pathogenicity and drug resistance cannot be seen immediately with our eyes when we observe a parasite in a test tube or under the microscope; therefore, we prefer to use morphological or molecular traits as a ‘number plate’ to recognize which group the respective individual belongs to. However, biodiversity is much more heterogeneous and complex than taxonomists want for their aim of classification, particularly in light of the fact that each individual differs from the other by thousands, if not tens of thousands, of different alleles [1]. Taxonomists have to find out which individuals, having one or a few traits in common, belong to a common species. If we are to encourage parasitologists into the species debate and the study of speciation, it is essential to provide the foundations. Otherwise, there is a serious danger of running into contradictions. Paul’s letter contains some contradictions. If a species is a ‘cross-section in an evolutionary lineage’, it cannot be at the same time, ‘a chunk of phylogenetic nexus’. http://parasites.trends.com
TRENDS in Parasitology Vol.18 No.10 October 2002
Which time interval is covered by this ‘cross-section’? One second, or a thousand years? Even during a short time interval, mutation and selection can change several traits in some individuals. Consequently, after a certain time, several genes and phenotypic characters are not the same as they were before. So, when does a species begin and when does it end? We cannot define a species as a slice of a sausage, while at the same time, we acknowledge its spatiotemporal dimension. Furthermore, what does ‘a single line of direct ancestry and descent’ mean? This would be easy to understand if we look at clonal propagation. But what are separate lineages in highly polymorphic populations? Are they gene lineages or lineages of species? These are not necessarily the same [2]. Sexuality, in addition, often ignores separate lineages because in certain groups of organisms, or under certain conditions, hybridization among different lineages occurs, resulting in genetic introgression of parts of the genome into non-directly related organisms. In several plants, in some animals, particularly in parasites, and, to a spectacular extent, in protists, new groups of organisms can arise by hybridization of distantly related groups, replacing the radiation principle of the evolutionary tree by a ‘modular principle’, contradicting the branching tree of Darwin and Haeckel [3]. Therefore, within certain limits, the formation of networks obscures proper lineages. Does Mayr’s biological species concept (population thinking) offer a solution? First, it is most important to discriminate between the properties of a population and those of its individuals. The properties of a population are, for example, population density or balanced polymorphism. The bearers of properties (such as colours, feathers, sexuality and reproduction) are not populations or reproductive communities, but only the individuals of populations. Individuals can mutate, populations cannot and, consequently, almost all the targets of selection are the traits of individuals, not those of the population. In other words, a population can evolve only in an indirect sense, namely as a consequence of the evolution of the individuals, which belong to that population [4]. Unfortunately, our daily language is not precise. We say that a certain species has a yellow bill. In fact, it is the individuals, not the species, which have a yellow bill. Under normal conditions, our abbreviated manner
of speaking is harmless because we are able to state it more precisely, if necessary. However, such manner of speaking can become dangerous, when we construct theories or definitions. With this intention, it is a logical mistake to attribute the properties of the members of a class to the class [4]. The species is not a material object. It is the result of a conceptual operation that combines individuals into a set in a mathematical sense. Of course, cladistic lineages and reproductive communities are real, but they are completely different from taxa. In some examples, a taxon can be understood as the transfer of such natural things into an artificial taxonomic system [5]. All real objects that will be used (and misunderstood) as species are only useful as an indicator for subsequent taxonomic classification. The reproductive community, for example, sometimes can be used to group individuals into a species taxon. However, in the majority of organismic biodiversity, particularly in plants, but also in several animal groups, a reproductive community either does not exist, or it represents a group of organisms that is not suited by any means to be used as a species taxon. Reproductive barriers are often not the cause of divergent evolution, nor are they essential for it to occur [6]. Also, sexual interaction is not a definition for a species because it does not tell us what a species is. Werner Kunz Section of Genetic Parasitology, Heinrich Heine University, Institute for Genetics, Universitätsstrasse 1, D-40225 Düsseldorf, Germany. e-mail: [email protected] References 1 Powell, J.R. (1997) Progress and Prospects in Evolutionary Biology – The Drosophila Model. Oxford University Press 2 Nichols, R. (2001) Gene trees and species trees are not the same. Trends Ecol. Evol. 16, 358–364 3 Doolittle, W.F. (1999) Phylogenetic classification and the universal tree. Science 284, 2124–2129 4 Mahner, M. and Bunge, M. (1997) Foundations of Biophilosophy. Springer-Verlag 5 Mahner, M. (1998) Why evolution still exists if species do not evolve. Theory Biosci. 117, 173–199 6 Mishler, B.D. and Donoghue, M.J. (1994) Species concepts: a case for pluralism. In: Conceptual Issues in Evolutionary Biology. (Sober, E. ed.), pp. 217–232, Massachusetts Institute of Technology Press
Published online: 21 August 2002
1471-4922/02/$ – see front matter © 2002 Elsevier Science Ltd. All rights reserved. PII: S1471-4922(02)02320-6
TRENDS in Parasitology Vol.18 No.10 October 2002
439
most appealing, it is essential to provide the necessary foundations. Although I appreciate that space limits could have prevented a more detailed discussion on this vast subject, with a little additional material, readers can be provided with a more complete picture and a more accessible bibliography. To provide readers with at least some context in this subject, it is therefore useful to consider the development of species thinking, particularly since the blossoming of evolutionary theory. Pre-darwinian approaches to species were based on Aristotle’s notion of ‘ideal’, where organisms have a natural state, and variation between organisms reflected the imperfection of nature. Such essentialist thinking defined species by individual characteristics that were both necessary and sufficient (i.e. species were considered as discrete units, where all members share a set of characters). Interestingly Aristotle’s concept on what characterizes an organism’s natural state was based on reproduction: fidelity of reproduction is a natural state of an organism. Such a discrete nature of a species, however, conflicts with darwinian theory, where evolution is considered a continuous process. Mayr’s biological species concept (BSC) offered an alternative to such essentialist thinking [9]. Although Mayr’s biological universal was also based on reproductive potential, it has one implicit but often unstated difference. What Mayr actually achieved was majestic; as an alternative to the individual-based approach, Mayr developed on a population-based approach. Evolutionary theory concerns itself with the properties of populations and the result of historical action on those properties. Rather than attempting to explain observed population phenomena by examining the characters of individual organisms, population thinking considers such phenomena as legitimate in their own right without trying to reduce them to the collective consequences of the individual (see Ref. [8]). By this, Mayr circumvented the problem inherent in the organismal level approach, wherein the criteria that specify when an organism belongs to a species instantly defines a group in terms of an individual property. The problem is what if local variation in a population confounds the criteria, even though the population
still belongs to the species (i.e. how to define the species in spite of natural variation?). Population thinking offered an alternative to such reductionism and brought species thinking in line with evolutionary theory. Since Mayr, there has been considerable debate and many developments in species thinking. As Kunz has pointed out, BSC excludes certain organisms (e.g. those reproducing clonally) and is often difficult to assess in many situations [1]. Incidentally, Kunz is incorrect in highlighting island populations as being automatically excluded from definition by BSC because Mayr stated ‘actually or potentially interbreeding populations’. On a final note, although it is now generally agreed that species are segments of population-level evolutionary lineages, there remains some debate over the value of having a species definition when aiming to understand the speciation process [10,11]. Understanding speciation and being able to define what constitutes a species is of paramount importance to parasitologists, especially those working in medical and veterinary parasitology. Certainly, species criteria could be different across parasitic taxa, but the extensive parasitological knowledge should enable parasitologists to make a valuable contribution to the species and speciation debate, as well as establishing practical criteria for pathogenic species identification.
Letters
Species concepts versus species criteria It was initially with great pleasure that I read the recent article of Werner Kunz addressing the issue of species, with respect to parasites [1]. However, despite a good introduction to this domain, this article side steps a rigorous analysis of the species problem: what is a species? This may not be surprising because it has been one of the most vexing issues in biology for decades. Kunz addresses all the relevant components of the species issue, discussing the problems of species diagnosis by using traits, the biospecies concept based on the capacity (trait) to interbreed, and goes as far as to introduce cladistics and classification according to evolutionary lineages. However, Kunz fails to resolve the important difference between concepts and criteria, which lies at the heart of the issue. Indeed, a recent discussion of this topic clearly indicates where the confusion lies [2,3]: there has been a tendency to confuse species concepts (ideas on the kind of entity that is designated a species category) and species criteria (the standard for judging whether an entity qualifies as a member of a species category). The species criteria provides a list on which to judge if groups of individuals are distinct species (e.g. there are intrinsic barriers to genetic exchange, species are diagnosable by fixed character states). The species concept should be concerned with defining a species according to some biological universal [4]. Although there have been a dozen or so suggested species concepts, all modern versions, including the cited Cracraft (1983) [5], are actually variations on a common theme of what designates a species – a group (population) of organisms occurring at a cross-section in an evolutionary lineage (where lineage is a single line of direct ancestry and descent). This idea was originally outlined by Ghiselin [6] and Hull [7]: organisms are conspecific by virtue of their actual historical relationships to each other and not according to their genotypic or phenotypic similarity (i.e. species are chunks of phylogenetic nexus [8], not natural kinds). If, as Kunz suggests, we are to encourage parasitologists into the species debate and the study of speciation, an idea that I find http://parasites.trends.com
Richard Paul Unité de Biochimie et Biologie Moléculaire des Insectes, Institut Pasteur, 28 rue du Dr. Roux, 75724 Paris cedex 15, France. e-mail: [email protected] References 1 Kunz, W. (2002) When is a parasite species a species? Trends Parasitol. 18, 121–124 2 de Queiroz, K. (1998) The general lineage concept of species, species criteria, and the process of speciation: a conceptual unification and terminological recommendations. In Endless Forms: Species and Speciation (Howard, D.J. and Belocher, S.H. eds), pp. 57–75, Oxford University Press 3 Harrison, R.G. (1998) Linking evolutionary pattern and process: the relevance of species concepts for the study of speciation. In Endless Forms: Species and Speciation (Howard, D.J. and Belocher, S.H. eds), pp. 19–31, Oxford University Press 4 Templeton, A.R. (1998) Species and speciation: geography, population structure, ecology, and gene trees. In Endless Forms: Species and Speciation (Howard, D.J. and Belocher, S.H. eds), pp. 32–43, Oxford University Press
1471-4922/02/$ – see front matter © 2002 Elsevier Science Ltd. All rights reserved. PII: S1471-4922(02)02319-X
440
News & Comment
5 Cracraft, J. (1983) Species concepts and speciation analysis. Curr. Ornithol. 1, 159–187 6 Ghiselin, M. (1974) A radical solution to the species problem. System. Zool. 23, 536–544 7 Hull, D. (1976) Are species really individuals? System. Zool. 25, 174–191 8 Sober, E. (1984) The Nature of Selection: Evolutionary Theory in Philosophical Focus, Massachusetts Institute of Technology Press 9 Mayr, E. (1963) Animal Species and Evolution, Belknap Press 10 Templeton, A.R. (1989) The meaning of species and speciation: a genetic perspective. In Speciation and its consequences (Otte, D. and Endler, J.A. eds), pp. 3–27, Sinauer 11 Bush, G.L. (1994) Sympatric speciation in animals: new wine in old bottles. Trends Ecol. Evol. 9, 285–288
Published online: 21 August 2002
Species concepts versus species criteria Response from Werner Kunz
Richard Paul’s letter is of great importance for parasitologists because it highlights the species debate. Within a group of similar parasitic individuals, some can be specific for one host, others for another; some can be pathogenic, others not; some can be sensitive to a drug and others are resistant. As a result of these data, individual parasites can be classified into groups. In several cases, host specificity, pathogenicity and drug resistance cannot be seen immediately with our eyes when we observe a parasite in a test tube or under the microscope; therefore, we prefer to use morphological or molecular traits as a ‘number plate’ to recognize which group the respective individual belongs to. However, biodiversity is much more heterogeneous and complex than taxonomists want for their aim of classification, particularly in light of the fact that each individual differs from the other by thousands, if not tens of thousands, of different alleles [1]. Taxonomists have to find out which individuals, having one or a few traits in common, belong to a common species. If we are to encourage parasitologists into the species debate and the study of speciation, it is essential to provide the foundations. Otherwise, there is a serious danger of running into contradictions. Paul’s letter contains some contradictions. If a species is a ‘cross-section in an evolutionary lineage’, it cannot be at the same time, ‘a chunk of phylogenetic nexus’. http://parasites.trends.com
TRENDS in Parasitology Vol.18 No.10 October 2002
Which time interval is covered by this ‘cross-section’? One second, or a thousand years? Even during a short time interval, mutation and selection can change several traits in some individuals. Consequently, after a certain time, several genes and phenotypic characters are not the same as they were before. So, when does a species begin and when does it end? We cannot define a species as a slice of a sausage, while at the same time, we acknowledge its spatiotemporal dimension. Furthermore, what does ‘a single line of direct ancestry and descent’ mean? This would be easy to understand if we look at clonal propagation. But what are separate lineages in highly polymorphic populations? Are they gene lineages or lineages of species? These are not necessarily the same [2]. Sexuality, in addition, often ignores separate lineages because in certain groups of organisms, or under certain conditions, hybridization among different lineages occurs, resulting in genetic introgression of parts of the genome into non-directly related organisms. In several plants, in some animals, particularly in parasites, and, to a spectacular extent, in protists, new groups of organisms can arise by hybridization of distantly related groups, replacing the radiation principle of the evolutionary tree by a ‘modular principle’, contradicting the branching tree of Darwin and Haeckel [3]. Therefore, within certain limits, the formation of networks obscures proper lineages. Does Mayr’s biological species concept (population thinking) offer a solution? First, it is most important to discriminate between the properties of a population and those of its individuals. The properties of a population are, for example, population density or balanced polymorphism. The bearers of properties (such as colours, feathers, sexuality and reproduction) are not populations or reproductive communities, but only the individuals of populations. Individuals can mutate, populations cannot and, consequently, almost all the targets of selection are the traits of individuals, not those of the population. In other words, a population can evolve only in an indirect sense, namely as a consequence of the evolution of the individuals, which belong to that population [4]. Unfortunately, our daily language is not precise. We say that a certain species has a yellow bill. In fact, it is the individuals, not the species, which have a yellow bill. Under normal conditions, our abbreviated manner
of speaking is harmless because we are able to state it more precisely, if necessary. However, such manner of speaking can become dangerous, when we construct theories or definitions. With this intention, it is a logical mistake to attribute the properties of the members of a class to the class [4]. The species is not a material object. It is the result of a conceptual operation that combines individuals into a set in a mathematical sense. Of course, cladistic lineages and reproductive communities are real, but they are completely different from taxa. In some examples, a taxon can be understood as the transfer of such natural things into an artificial taxonomic system [5]. All real objects that will be used (and misunderstood) as species are only useful as an indicator for subsequent taxonomic classification. The reproductive community, for example, sometimes can be used to group individuals into a species taxon. However, in the majority of organismic biodiversity, particularly in plants, but also in several animal groups, a reproductive community either does not exist, or it represents a group of organisms that is not suited by any means to be used as a species taxon. Reproductive barriers are often not the cause of divergent evolution, nor are they essential for it to occur [6]. Also, sexual interaction is not a definition for a species because it does not tell us what a species is. Werner Kunz Section of Genetic Parasitology, Heinrich Heine University, Institute for Genetics, Universitätsstrasse 1, D-40225 Düsseldorf, Germany. e-mail: [email protected] References 1 Powell, J.R. (1997) Progress and Prospects in Evolutionary Biology – The Drosophila Model. Oxford University Press 2 Nichols, R. (2001) Gene trees and species trees are not the same. Trends Ecol. Evol. 16, 358–364 3 Doolittle, W.F. (1999) Phylogenetic classification and the universal tree. Science 284, 2124–2129 4 Mahner, M. and Bunge, M. (1997) Foundations of Biophilosophy. Springer-Verlag 5 Mahner, M. (1998) Why evolution still exists if species do not evolve. Theory Biosci. 117, 173–199 6 Mishler, B.D. and Donoghue, M.J. (1994) Species concepts: a case for pluralism. In: Conceptual Issues in Evolutionary Biology. (Sober, E. ed.), pp. 217–232, Massachusetts Institute of Technology Press
Published online: 21 August 2002
1471-4922/02/$ – see front matter © 2002 Elsevier Science Ltd. All rights reserved. PII: S1471-4922(02)02320-6