Species and the Species Problem

1.1. Species as the Basic Unit of Biological Diversity

Species occupies a special position in the system of biological knowledge. It is not simply one of many taxonomic categories—it is a fundamental unit with which all biological disciplines work, and agronomy is no exception (Simpson, 2018; Stuessy, 2009). When an agronomist encounters a plant disease, a pest, or a weed, the first practical question to answer is: “What is this organism?” Without answering this question, it is impossible either to correctly diagnose the problem or to select effective control measures.

Species is the basic structural unit in the system of living organisms, possessing a sexual process, a special qualitative stage of evolution, and at the same time—the basic taxonomic category (Naida, 2021). It is species that serves as the “building block” from which the entire hierarchical classification is constructed: genera unite species, families unite genera, orders unite families, and so on (Pandey, 2021). Without a clear understanding of what a species is and where its boundaries lie, no practical activity related to the identification of organisms is possible.

In the agrosphere, the importance of species can hardly be overestimated. Determining the species of a pathogen underlies disease diagnosis (Agrios, 2005; Sokirko, 2019). Establishing the species of a pest determines the choice of insecticide and protection strategy (Zakhvatkin, 2001). Identifying the species of a weed affects the choice of herbicide and tillage system. Finally, the species of a cultivated plant is the unit with which breeders work when creating new cultivars (Stuessy, 2009).

However, this is where the problem begins. An agronomist needs a clear, unambiguous answer to the question “What is this organism?”, but science cannot always provide such an answer. This contradiction between the practical need for certainty and the scientific complexity of real biological diversity constitutes the essence of the species problem—one of the most debated topics in biology (Pavlinov, 2023; Zachos, 2018).

1.2. The Paradox of Practical Identification

The paradox is as follows. On the one hand, species is something that “everyone knows” and “everyone can recognize.” Since ancient times, people have distinguished “species” of plants and animals: oak, birch, wolf, hare—these categories are intuitively understandable and are used in everyday life. Moreover, anthropological studies show that representatives of traditional cultures identify species that in most cases coincide with scientific ideas (Stuessy, 2009). On the other hand, on closer examination it turns out that boundaries between species are often blurred, and reliable delimitation requires the use of complex methods—genetic, cytological, ecological, biochemical.

The problem is compounded by the fact that in nature there exist groups of organisms that are morphologically practically indistinguishable but at the same time represent genetically isolated, independent evolutionary lineages. Such groups are called cryptic species or sibling species (Stuessy, 2009; Simpson, 2018). For the agrosphere, this has direct practical significance: if two cryptic species differ in resistance to pesticides, in the spectrum of affected crops, or in pathogenicity, then an error in identification leads to an error in protective measures.

1.3. Examples from the Agrosphere: Cryptic Species in Insects

A classic example of cryptic species in entomology is the complex Drosophila pseudoobscura and D. persimilis. These two species of dipteran insects are morphologically practically indistinguishable, but differ in wing size (variation in the wing index: from 45.7 to 62.8 in the first species and from 68.8 to 76.2 in the second) and, more importantly, are reproductively isolated (Zakhvatkin, 2001). For an agronomist, this example is important as an illustration of a general principle: morphological similarity does not guarantee taxonomic unity.

A more agrosphere-related example is the grain moth (Tinea granella), which, as it turned out, represents a complex of four species, of which only two are harmful (Zakhvatkin, 2001). The leafroller Choristoneura fumiferana is divided into two species according to the nature of its food specialization. Among Coleoptera, an example is the rice and granary weevils (Sitophilus oryzae and S. zeamais), which for a long time were considered one species Calandra oryzae—one of them feeds on maize, the second on wheat (Zakhvatkin, 2001). Sibling species have also been recorded in Orthoptera, some ants, aphids, and springtails.

For plant protection practice, this means that identifying a pest “to species” on the basis of morphological characters alone may be insufficient. If two sibling species differ in resistance to an insecticide or in phenology, the control strategy must take this difference into account. However, to reveal it, additional methods are needed—genetic, biochemical, behavioral.

1.4. Examples from the Agrosphere: Cryptic Species in Fungi

In mycology, the problem of cryptic species is especially acute, since morphological characters of fungi are often limited and plastic (Taylor et al., 2000; Webster & Weber, 2007). A classic example is Armillaria mellea sensu lato (honey fungus), which, as it turned out, represents a complex of more than a dozen species differing in biology, ecology, and pathogenicity (Taylor et al., 2000). For an agronomist, this means that the “honey fungus” on different crops or in different regions may be a different species with a different control strategy.

Another example is Gibberella fujikuroi (teleomorph of Fusarium), a complex in which molecular-phylogenetic methods revealed 45 species, of which 23 turned out to be new to science (O'Donnell et al., 1998; Taylor et al., 2000). Many of these species differ in the spectrum of affected crops and in the mycotoxins they produce. For practice, this means that identifying “Fusarium wilt” without specifying the particular pathogen species may be insufficient for choosing a protection strategy and for assessing the risk of mycotoxin contamination of products.

An even more illustrative example is Histoplasma capsulatum—the causative agent of human histoplasmosis, which, as it turned out, represents a complex of six genetically isolated groups correlating with geographic distribution and pathogenicity (Kasuga et al., 1999; Taylor et al., 2000). Although this example belongs to medical mycology, it illustrates a general principle: a morphological species may conceal several evolutionarily independent lineages.

In phytopathology, an analogous situation is observed with Coccidioides immitis—the causative agent of coccidioidomycosis, in which two cryptic species have been revealed, differing in geographic distribution (California vs. other regions) and in some physiological properties (Koufopanou et al., 1997; Taylor et al., 2000). For the agrosphere, this means that even within one “morphological species” of a pathogen there may exist groups differing in aggressiveness, host range, or resistance to fungicides.

1.5. Examples from the Agrosphere: Cryptic Species in Nematodes

Nematodes are another group in which cryptic species occur especially often. Morphological characters of nematodes are limited, and many species considered cosmopolitan, upon genetic analysis, break up into complexes of cryptic species (Stuessy, 2009). For the agrosphere, this is directly relevant: for example, root-knot nematodes (Meloidogyne spp.)—one of the most harmful plant pathogens—represent a complex of species differing in the spectrum of affected crops and in resistance to nematicides. Identifying a nematode species solely by morphology may be insufficient for choosing a protection strategy.

1.6. Why Species Is a Hypothesis, Not a Fact

Modern systematics regards species not as a static, once-and-for-all established unit, but as a scientific hypothesis about the boundaries of an evolutionarily independent lineage (Stuessy, 2009; Zachos, 2018). This is a fundamentally important position. A hypothesis can be confirmed, refined, or refuted as new data accumulate—morphological, molecular, ecological, cytogenetic.

From this follow important practical conclusions. First, species names may be revised as new data accumulate. What yesterday was considered one species may today be divided into several, and vice versa—what was considered different species may be united. Second, different sources of information—identification keys, databases, molecular phylogenies—may give different answers to the question of species boundaries. Third, practical identification always requires critical thinking and an understanding of which species concept a particular identification key or database uses (Zachos, 2018).

An example from the agrosphere: in phytopathology, until recently Pseudomonas syringae was regarded as one species with many pathovars. However, molecular studies showed that it is a complex of several genetically distinct groups, which led to a revision of the taxonomy and, accordingly, to changes in pathogen names (Sigee, 1993). For practice, this means that the pathogen name in an old identification key may not correspond to modern taxonomy, and this must be taken into account in diagnosis.

1.7. Species as a Central Concept and a Source of Problems

Thus, species is simultaneously a central concept of biology and a source of constant debate. The centrality of species is due to the fact that it is the basic unit of biological diversity with which all biological disciplines, including agronomy, work. The problematic nature of species is due to the fact that real biological diversity does not always fit into clear discrete categories: there exist cryptic species, hybrids, polyploids, apomicts, asexual organisms, prokaryotes with horizontal gene transfer—and for all these cases the classical concept of species requires refinement or modification (Doolittle & Papke, 2006; Van Regenmortel, 2010; Zachos, 2018).

For an agronomist, it is important to understand that species is not a “label” that can be mechanically attached to an organism, but a scientific hypothesis requiring verification and refinement. In practical work, this means the necessity of an integrated approach to identification: morphological characters must be combined with ecological, physiological, and, where possible, molecular-genetic data. Only such an approach allows minimizing errors that in the agrosphere can have serious economic and ecological consequences.

1.8. Chapter Summary

1. Species is the basic unit of biological diversity and practical identification of organisms. For agronomy, accurate determination of the species of a pathogen, pest, or cultivated plant is critically important.

2. There is a paradox: an agronomist needs a clear answer to the question “What is this organism?”, but science cannot always give an unambiguous answer because of the complexity of real biological diversity.

3. Cryptic species (sibling species)—morphologically indistinguishable but genetically and ecologically distinct groups—occur in insects, fungi, nematodes, and other organisms important for the agrosphere.

4. In modern systematics, species is regarded as a scientific hypothesis, not as a static unit. Species boundaries may be revised as new data accumulate.

5. For practical identification, an integrated approach is needed, combining morphological, ecological, physiological, and molecular-genetic methods.

2.1. Introduction: The Polysemy of the Word “Species”

The word “species” is polysemous. In everyday speech it means “external appearance,” “variety,” “sort,” “breed.” We say “type of goods,” “type of sport,” “residence permit.” In biology, however, the term “species” (Latin species) has a strictly defined, although not unique, meaning. It is simultaneously a taxonomic category—a level in the hierarchy of the living—and a concrete taxon—a group of organisms to which a name has been assigned (Stuessy, 2009; Van Regenmortel, 2010).

Such polysemy creates difficulties not only in scientific literature but also in the practical work of an agronomist. When plant protection recommendations indicate “pest species,” it is important to understand what exactly is meant: a taxonomic species in the strict sense, an economically biological category (for example, a pathogen race), or a morphologically similar group that in another identification key may be called differently. Therefore, it is necessary to clearly distinguish the levels of understanding of species: everyday, scientific-categorical, and scientific-taxonomic (Pavlinov, 2023; Zachos, 2018).

2.2. The Everyday Understanding of Species

The everyday, or folk, understanding of species is formed spontaneously, on the basis of external characters, practical significance, and cultural context. Since ancient times, people have distinguished “species” of plants and animals: oak, birch, wolf, hare—these categories are intuitively understandable and used in everyday life. Anthropological studies show that representatives of traditional cultures identify groups of organisms that in most cases coincide with scientific species. For example, one Papuan tribe recognized 136 names for 137 bird species known to modern science (Stuessy, 2009). This means that everyday thinking is capable of grasping real discontinuities in biological diversity.

However, the everyday understanding of species has significant limitations. First, it is based primarily on external, easily observable characters that may not reflect the genetic and evolutionary independence of a group. Second, it is closely tied to the economic usefulness or harmfulness of an organism, which leads to a confusion of taxonomic and utilitarian categories. Third, everyday thinking tends toward typologization: a species is perceived as a “type,” a “standard,” and deviations from it as random anomalies (Stuessy, 2009; Pavlinov, 2023).

In the agrosphere, the everyday understanding of species manifests itself in the use of terms such as “cultivar,” “breed,” “race,” “strain.” These categories are not taxonomic species, but in everyday practice they are often equated with or confused with species. For example, a “race” of a phytopathogen is an intraspecific group differing in virulence to certain cultivars, not a taxonomic species (Agrios, 2005; Sokirko, 2019). Similarly, a “cultivar” of a cultivated plant is an artificially bred assemblage, not a natural species (Naida, 2021). A clear distinction between these concepts is necessary for correct diagnosis and choice of protection strategy.

2.3. Scientific Understanding: Two Levels

Scientific understanding of species includes two interrelated but distinct levels: species as a category and species as a taxon.

Species as a category (species category) is an abstract concept denoting a certain rank in hierarchical classification. Along with the categories “genus,” “family,” “order,” the category “species” has no concrete spatiotemporal referents; it exists only in the researcher’s mind as a tool for ordering diversity (Van Regenmortel, 2010; Stuessy, 2009). The category “species” answers the question “what level of organization do we call a species?” but not the question “which particular organisms belong to a given species?”

Species as a taxon (species taxon) is a concrete group of organisms to which a name has been assigned. For example, Homo sapiens, Quercus robur, Fusarium oxysporum are species taxa. A taxon has real members—organisms possessing certain properties. The connection between category and taxon is realized through the relation of inclusion: the taxon Quercus robur is included in the category “species” (Van Regenmortel, 2010; Stuessy, 2009).

Distinguishing these levels is fundamentally important. When we say “species is the basic unit of classification,” we mean the category. When we say “this species is distributed in Europe,” we mean the taxon. Confusing these levels generates many logical and practical errors. For example, the statement “the species has changed” may mean either a change in ideas about the boundaries of the taxon (a revision of systematics) or a real evolutionary change in the group of organisms. These are different things, and they must be distinguished (Stuessy, 2009; Zachos, 2018).

Moreover, species can be considered as a category of thought (a mental construct) and as a really existing group (an evolutionary lineage). In the first case, species is a class, a set defined through a set of characters. In the second case, species is a population system, an ancestro-descendant lineage existing in space and time independently of whether we recognize it or not. Modern systematics recognizes both aspects: species is both a mental construction and a real evolutionary unit (Van Regenmortel, 2010; Stuessy, 2009).

The American systematist Tod F. Stuessy (Stuessy, 2009) distinguishes three kinds of reality of species:

1. Mental reality—species as a concept existing in the researcher’s consciousness. Practically all biologists, including nominalists, agree with this.

2. Biological reality—species as a group of organisms connected by common descent and (for sexual organisms) by interbreeding. The existence of biological reality is recognized by the majority but disputed by extreme nominalists.

3. Evolutionary reality—species as a product and participant in the evolutionary process. If a species is biologically real, then it is also evolutionarily real.

Such a three-level understanding allows avoiding the extremes of nominalism (species is only a speculative construction) and naive realism (species is an immutable essence, given once and for all). Species is simultaneously constructed by our thinking and reflects real discontinuities of living nature (Stuessy, 2009; Pavlinov, 2023).

2.4. Historical View: From Linnaeus to Population Thinking

The history of understanding species spans more than two millennia and reflects the development not only of biology but also of philosophy and general scientific methodology (Pavlinov, 2023; Stuessy, 2009).

Antiquity and the Middle Ages. Plato introduced the concept of “eidos” (idea, form)—an eternal and immutable prototype to which all concrete things correspond. Aristotle developed the doctrine of logical division: species is a unit possessing a common essence, defined through genus and specific difference. In medieval scholasticism, species was understood as a universal—either real (realism) or speculative (nominalism). These philosophical disputes laid the foundation for the future species problem (Pavlinov, 2023; Stuessy, 2009).

Carl Linnaeus (1707–1778). Linnaeus created the system of binomial nomenclature and hierarchical classification that still underlies systematics. His understanding of species was typological and creationist: species were created by God, immutable and fixed. Each species has its own “essence,” and deviations are random variations not deserving taxonomic recognition. Linnaeus allowed the existence of varieties but regarded them as the result of environmental influence, not as evolutionary changes. His famous formula “Tot numeramus species, quot ab initio creavit infinitum Ens” (“We count as many species as the Infinite Being created initially”) expresses the essence of typological thinking (Stuessy, 2009; Pavlinov, 2023).

John Ray (1627–1705). Ray, a predecessor of Linnaeus, approached species more natural-scientifically. He defined species through the ability to produce offspring from seed and considered species real but not necessarily immutable. His approach combined morphological and reproductive criteria, which anticipated future biological concepts (Stuessy, 2009).

Charles Darwin (1809–1882). Darwin radically changed the understanding of species. In “On the Origin of Species” (1859) he showed that species are not fixed essences but arise and change in the process of evolution. Darwin believed that boundaries between species are blurred and that the concept of species itself is largely conventional: “I look at the term ‘species’ as one arbitrarily given, for the sake of convenience, to a set of individuals closely resembling each other, and that it does not essentially differ from the term ‘variety’” (cited in Stuessy, 2009). However, Darwin did not deny the reality of species as temporary evolutionary units; he emphasized their variability and origin from a common ancestor. His ideas laid the foundation for the evolutionary approach to species (Stuessy, 2009; Pavlinov, 2023).

After Darwin: Population Thinking. In the late 19th and early 20th centuries, the development of genetics, cytology, and population biology led to the formation of population thinking. Species began to be regarded not as a collection of individuals corresponding to a “type” but as a collection of populations connected by a common gene pool. Important roles were played by the works of E. Mayr, F. Dobzhansky, J. Huxley, and other representatives of the synthetic theory of evolution (Stuessy, 2009; Simpson, 2018).

Ernst Mayr (1904–2005) and the Biological Species Concept. Mayr formulated the biological species concept (BSC): “Species are groups of actually or potentially interbreeding natural populations that are reproductively isolated from other such groups” (Mayr, 1942; cited in Stuessy, 2009). This concept focuses on reproductive isolation as the key criterion of species. It became dominant in zoology and for a long time was widely accepted in botany. However, BSC has limitations: it is inapplicable to asexual organisms, prokaryotes, fossil forms, and in plants reproductive isolation is often incomplete because of hybridization (Stuessy, 2009; Simpson, 2018).

Modern Concepts. In the second half of the 20th century, many alternative species concepts appeared: evolutionary (Simpson, 1961; Wiley, 1978), phylogenetic (Cracraft, 1983; Nixon & Wheeler, 1990), genetic (Wu, 2001), ecological (Van Valen, 1976), cohesion (Templeton, 1989), genealogical (Baum & Shaw, 1995), and others (Pandey, 2021; Simpson, 2018). Each emphasizes one or another aspect: evolutionary independence, monophyly, ecological niche, genetic distinctness. The diversity of concepts reflects the complexity of real biological diversity and the impossibility of reducing it to one universal definition (Zachos, 2018; Pavlinov, 2023).

2.5. Species as a Category of Thought and as a Really Existing Group

The question of whether species is only a category of thought or a really existing group is a philosophical question with direct practical consequences. If species is only a speculative construction, then any boundaries between species are subjective and arbitrary. If species is real, then boundaries are objective and can be discovered rather than invented (Stuessy, 2009; Pavlinov, 2023).

Modern systematics takes an intermediate position. On the one hand, species is a mental construct, since we delimit species on the basis of our ideas about characters and criteria. On the other hand, species reflects real discontinuities of living nature that arose in the course of evolution. These discontinuities are not always clear and unambiguous—they may be blurred, especially in plants, fungi, and bacteria. But they are real in the sense that they exist independently of our consciousness (Van Regenmortel, 2010; Stuessy, 2009).

An important consequence: species is a scientific hypothesis, not a fact. Species boundaries are established on the basis of available data and may be revised as new data accumulate. For example, molecular-genetic methods have made it possible to reveal cryptic species where morphological analysis saw no differences (Taylor et al., 2000; Doolittle & Papke, 2006). This means that species are not “eternal” and “immutable” units; they are working tools that are refined as science develops (Zachos, 2018).

For an agronomist, this has direct practical significance. Identification keys and databases used by an agronomist may be based on different species concepts and, consequently, give different names for the same organisms. For example, in phytopathology until recently Pseudomonas syringae was regarded as one species with many pathovars; modern molecular studies have shown that it is a complex of several genetically distinct groups, which has led to a revision of the taxonomy (Sigee, 1993). Similarly, in mycology many morphological species have broken up into complexes of cryptic species (Taylor et al., 2000). Therefore, practical identification always requires critical thinking and an understanding of which species concept a particular source of information uses (Zachos, 2018; Stuessy, 2009).

2.6. Chapter Summary

1. The word “species” is polysemous. In biology, a distinction is made between species as a category (an abstract level of classification) and species as a taxon (a concrete group of organisms).

2. The everyday understanding of species is based on external characters and practical significance. It may coincide with the scientific one, but it does not guarantee accuracy and does not distinguish taxonomic and economic categories.

3. Scientific understanding of species includes three aspects of reality: mental, biological, and evolutionary. Species is simultaneously constructed by thought and reflects real discontinuities of nature.

4. Historically, the understanding of species has passed from typological and creationist (Linnaeus) through evolutionary (Darwin) to population and the modern multiplicity of concepts (Mayr and others).

5. Species is a scientific hypothesis, not a static fact. Species boundaries may be revised as new data accumulate, which has direct consequences for practical identification in the agrosphere.

3.1. Introduction: The Diversity of Concepts as a Reflection of Nature’s Complexity

In previous chapters we established that species is a central but problematic concept of biology. One of the main reasons for this problematic nature is the existence of many competing species concepts. The number of proposed concepts runs into dozens: by various estimates, from 20 to 34 or more (Mayden, 1997; Zachos, 2018). Such diversity is not a sign of weakness in science but a reflection of the real complexity of biological diversity. Different groups of organisms (plants, fungi, bacteria, animals) possess different biological characteristics, and a universal definition of species that would work equally well for all proves unattainable (Stuessy, 2009; Pavlinov, 2023).

Each species concept offers its own criterion for delimiting species. Some concepts emphasize reproductive isolation, others morphological distinctness, others monophyly, others ecological niche. The choice of concept has not only theoretical but also practical significance: it determines how many species we will delimit in the group under study, which characters we will use for diagnosis, and how we will interpret boundaries between taxa (Zachos, 2018; Simpson, 2018).

In this chapter we will examine the main species concepts, their advantages and limitations, and their applicability to different groups of organisms important for the agrosphere. We will follow this logic: first we will consider the most traditional concepts (morphological and biological), then move to phylogenetic and evolutionary, and after that to ecological and genetic. We will conclude with a comparison of concepts and a discussion of their practical significance for agronomy.

3.2. The Morphological (Typological) Species Concept

Definition and essence. The morphological species concept (MSC) is historically the first and most intuitively understandable. According to it, a species is a group of organisms that are morphologically similar to one another and differ from other such groups by certain characters. The classic definition belongs to the American botanist Arthur Cronquist: “Species are the smallest groups that are consistently and persistently distinct and distinguishable by ordinary means” (Cronquist, 1978; cited in Stuessy, 2009). In a stricter formulation, a morphological species is “the smallest natural population permanently separated from another such population by a gap in the series of biotypes” (Du Rietz, 1930; cited in Stuessy, 2009).

MSC is based on the idea that species are real and discrete, and their boundaries can be established by morphological gaps. If between two groups of organisms there exists a stable morphological gap not filled by intermediate forms, these groups are recognized as different species. If the differences are gradual and overlap, the groups are considered one species (Stuessy, 2009).

Advantages of MSC. The morphological concept has a number of undeniable merits:

1. Practicality. It does not require complex experiments or molecular analyses; to determine a species it is enough to study the external and internal structure of the organism.

2. Universality. It is applicable to any organisms, including fossils, asexual forms, prokaryotes, and viruses, for which other concepts do not work.

3. Historical continuity. Most described species were delimited precisely on the basis of the morphological criterion; therefore MSC underlies existing nomenclature.

4. Connection with other characters. In most cases morphological gaps correlate with genetic and ecological differences, since morphology reflects adaptations and evolutionary history (Stuessy, 2009; Simpson, 2018).

Limitations of MSC. However, the morphological concept also has significant shortcomings:

1. Subjectivity. The decision as to which morphological gap is sufficient to delimit a species is often subjective and depends on the experience and views of the researcher.

2. Cryptic species. There exist genetically isolated species that are morphologically practically indistinguishable (sibling species). MSC does not allow their detection (Taylor et al., 2000; Zakhvatkin, 2001).

3. Polymorphism. One and the same species may have different morphological forms (for example, sexual dimorphism, seasonal polymorphism, ecological races). MSC may erroneously divide such a species into several.

4. Hybridization. During hybridization, morphological boundaries between species are blurred, which complicates the application of MSC (Stuessy, 2009).

5. Ignoring biological essence. MSC does not take into account reproductive and evolutionary aspects that for many biologists are key in defining species.

Applicability in the agrosphere. Despite its limitations, MSC remains the most widely used concept in practical agronomy and phytopathology. Identification keys for plants, insects, fungi, and nematodes used by agronomists are built primarily on morphological characters. This is explained by the accessibility of the method and the possibility of rapid diagnosis in field conditions. However, where the morphological method fails (for example, with cryptic species of pathogens or pests), additional approaches must be involved (Sokirko, 2019; Zakhvatkin, 2001).

3.3. The Biological (Isolation) Species Concept

Definition and essence. The biological species concept (BSC) was formulated by Ernst Mayr in 1942: “Species are groups of actually or potentially interbreeding natural populations that are reproductively isolated from other such groups” (Mayr, 1942; cited in Stuessy, 2009). The key criterion here is reproductive isolation: if two groups of organisms do not interbreed in nature or produce sterile offspring, they are considered different species. If they interbreed and produce fertile offspring, they belong to one species.

BSC focuses on the gene pool as the basis of species unity. A species is a “reproductive community” whose members exchange genes and are isolated from other such communities. Reproductive isolation may be due to different mechanisms: geographic isolation, different flowering times, incompatibility of pollen and stigma, sterility of hybrids, and so on (Stuessy, 2009; Simpson, 2018).

Advantages of BSC. The biological concept was for a long time considered the most theoretically justified:

1. Biological essence. It defines species through real biological processes—interbreeding and isolation—rather than through external characters.

2. Objectivity of criterion. Reproductive isolation is a discrete character: organisms either interbreed or not. This reduces subjectivity compared with the morphological approach.

3. Evolutionary interpretation. BSC agrees well with evolutionary theory: reproductive isolation is a key stage of speciation.

4. Practical testability. In some cases the presence of reproductive isolation can be tested experimentally (for example, in laboratory crosses).

Limitations of BSC. However, BSC faces serious difficulties:

1. Asexual organisms. BSC is inapplicable to organisms reproducing asexually (bacteria, many fungi, some plants and animals). For them the concept of “interbreeding” is meaningless.

2. Prokaryotes. In bacteria, horizontal gene transfer and the absence of a sexual process make BSC inapplicable (Doolittle & Papke, 2006).

3. Fossils. For extinct organisms it is impossible to test reproductive isolation.

4. Hybridization. In plants, interspecific hybridization is a common phenomenon. Many plant species interbreed and produce fertile offspring but at the same time retain their integrity. BSC does not work in such cases (Stuessy, 2009).

5. Geographic isolation. If populations are geographically isolated but potentially capable of interbreeding, BSC considers them one species. However, in practice such populations are often independent evolutionary lineages, and their union into one species may be unjustified (Zachos, 2018).

6. Practical difficulty. Testing reproductive isolation in nature is often impossible or extremely laborious. For most organisms such data are absent.

Applicability in the agrosphere. BSC has limited application in agronomy. For cultivated plants reproducing by seed, it may be useful in determining boundaries between wild relatives, but for most pathogens (fungi, bacteria, viruses) and pests (insects with asexual reproduction) it does not work. Nevertheless, understanding reproductive isolation is important for breeding: when crossing cultivated plants with wild relatives, it is necessary to take into account the possibility of obtaining fertile offspring. In addition, BSC underlies many theoretical ideas about speciation that are used in breeding for resistance (Stuessy, 2009; Agrios, 2005).

3.4. The Phylogenetic Species Concept

Definition and essence. The phylogenetic species concept (PSC) arose within cladistics. It exists in several variants, but common to them is the requirement that a species be a monophyletic group—that is, include all descendants of one common ancestor. In addition, the species must be diagnosable—that is, possess a unique combination of characters (apomorphies) distinguishing it from other species (Cracraft, 1983; Nixon & Wheeler, 1990; Simpson, 2018).

One variant of PSC, proposed by Nixon and Wheeler (Nixon & Wheeler, 1990), defines a species as “the smallest aggregation of populations or lineages diagnosable by a unique combination of character states in comparable individuals.” Another variant, proposed by Cracraft (Cracraft, 1983), emphasizes monophyly: a species is “the smallest diagnosable cluster of individual organisms within which there is a parental pattern of ancestry and descent.”

Advantages of PSC.

1. Consistency with phylogenetics. PSC fits naturally into modern phylogenetic systematics based on the reconstruction of evolutionary relationships.

2. Applicability to any organisms. PSC does not require sexual reproduction, so it is applicable to asexual forms, prokaryotes, and fossils (given sufficient data).

3. Diagnosability. The requirement of a unique combination of characters makes species boundaries clearer and more testable.

4. Consideration of evolutionary history. PSC strives to reflect real evolutionary lineages, not only external similarity.

Limitations of PSC.

1. The problem of monophyly at the species level. Many species are not monophyletic in the strict sense because of hybridization, introgression, and incomplete lineage sorting. This is especially characteristic of plants (Stuessy, 2009; Simpson, 2018).

2. Subjectivity of diagnostic characters. The choice of characters for species diagnosis may be arbitrary; different researchers may delimit different numbers of species on the basis of the same data.

3. Species splitting. PSC often leads to the delimitation of more species than BSC or MSC. This may create practical inconveniences, especially in the agrosphere, where stability of names is important.

4. Non-operationality for some groups. For many groups (for example, microorganisms) phylogenetic data may be incomplete or contradictory.

Applicability in the agrosphere. PSC is becoming increasingly widespread in phytopathology and mycology, where molecular-phylogenetic methods make it possible to reveal cryptic species and refine pathogen boundaries. For example, in the Gibberella fujikuroi complex (anamorph Fusarium), phylogenetic analysis revealed 45 species instead of one morphological species (O'Donnell et al., 1998; Taylor et al., 2000). This has direct practical significance: different species may differ in pathogenicity, host range, and sensitivity to fungicides. However, widespread introduction of PSC into practice requires training specialists and the availability of molecular laboratories.

3.5. The Evolutionary Species Concept

Definition and essence. The evolutionary species concept (ESC) was proposed by George Gaylord Simpson in 1951 and refined in 1961: “An evolutionary species is a lineage (an ancestral-descendant sequence of populations) evolving separately from other such lineages and possessing its own evolutionary tendencies and historical fate” (Simpson, 1961; cited in Stuessy, 2009). Later Wiley (Wiley, 1978) refined this definition by adding the requirement of maintaining identity and having its own historical fate.

ESC emphasizes the evolutionary independence of a lineage. A species is not simply a group of similar organisms but a historical entity having a beginning, development, and (potentially) an end. The criterion of species is not so much morphological similarity or reproductive isolation as the uniqueness of the evolutionary trajectory.

Advantages of ESC.

1. Universality. ESC is applicable to all organisms, including asexual forms, prokaryotes, and fossils, since it does not require interbreeding.

2. Consideration of the temporal aspect. ESC regards species as a dynamic unit, which corresponds to modern ideas about evolution.

3. Integrativeness. ESC can include other criteria (morphological, genetic, ecological) as evidence of evolutionary independence.

4. Theoretical depth. ESC most adequately reflects the ontological status of species as a real evolutionary unit.

Limitations of ESC.

1. Non-operationality. The main shortcoming of ESC is the absence of clear operational criteria. How can one determine whether a given group possesses “its own evolutionary fate”? This requires knowledge of evolutionary history, which is often unavailable.

2. Practical difficulty. To apply ESC it is necessary to reconstruct phylogeny and assess the degree of genetic and ecological distinctness, which requires great effort.

3. Subjectivity. The decision as to whether a given lineage is sufficiently independent to be recognized as a species is often subjective.

Applicability in the agrosphere. ESC is rarely used in practical agronomy directly because of its non-operationality. However, its ideas underlie many modern approaches to defining species, especially in the context of biodiversity conservation and understanding evolutionary processes. For an agronomist it is important to understand that species is not a static unit but a dynamic lineage, which matters in predicting the emergence of new pathogen races and the adaptation of pests.

3.6. The Ecological Species Concept

Definition and essence. The ecological species concept (EcSC) was proposed by Leigh Van Valen in 1976: “A species is a lineage (or a closely related set of lineages) which occupies an adaptive zone minimally different from that of any other lineage in its range and which evolves separately from all lineages outside its range” (Van Valen, 1976; cited in Stuessy, 2009). The key criterion here is the ecological niche: a species is a group of organisms occupying a certain adaptive zone and differing from other groups in ecological requirements.

EcSC emphasizes the role of natural selection and ecological factors in the formation and maintenance of species. Species differ not only genetically but also ecologically; they occupy different niches and compete with one another.

Advantages of EcSC.

1. Ecological interpretation. EcSC links species with real ecological conditions, which is important for understanding adaptations.

2. Applicability to asexual organisms. Like ESC, EcSC does not require sexual reproduction.

3. Practical significance. For the agrosphere, the ecological criterion is directly relevant: species of pests and pathogens differ in the spectrum of affected crops, in resistance to environmental factors, and in phenology. These differences underlie plant protection strategies.

Limitations of EcSC.

1. Difficulty of defining the niche. The ecological niche is a multidimensional concept, and its precise definition is often difficult.

2. Niche overlap. Many species occupy overlapping niches, which complicates delimitation.

3. Subjectivity. The choice of ecological characters for delimiting species may be arbitrary.

4. Inapplicability to some groups. For organisms lacking clear ecological specialization (for example, many saprotrophs), EcSC is not very informative.

Applicability in the agrosphere. The ecological concept is widely used in agronomy to delimit ecological races, pathotypes, and biotypes. For example, in phytopathology, pathogen races are distinguished by their virulence to certain cultivars; these races often correspond to ecological groups adapted to certain conditions. However, it is important to remember that a race is not a taxonomic species but an intraspecific category, and its delimitation is based on the ecological criterion (Agrios, 2005; Sokirko, 2019).

3.7. The Genetic (Gene) Species Concept

Definition and essence. The genetic species concept (GSC) defines species through genetic distinctness. According to it, a species is a group of populations that are genetically isolated from other such groups and have a common gene pool. In a stricter formulation proposed by Wu (Wu, 2001), a species is “the assemblage of all individuals having a common genetic pool that is isolated from other such pools.” The genetic concept is closely related to the biological one but emphasizes not reproductive isolation as such but genetic differentiation.

Advantages of GSC.

1. Molecular basis. With the development of molecular methods, GSC has received a powerful toolkit for quantitative assessment of genetic differences.

2. Applicability to microorganisms. For bacteria and fungi, where BSC does not work, genetic criteria (for example, the level of DNA similarity) have become the standard for delimiting species.

3. Objectivity. Genetic data may be more objective than morphological data, since they directly reflect the genotype.

Limitations of GSC.

1. The threshold problem. What level of genetic differences is sufficient to delimit a species? There is no single answer; different thresholds are used for different groups of organisms.

2. Horizontal transfer. In bacteria, horizontal gene transfer can lead to mosaic genomes, which complicates the application of GSC (Doolittle & Papke, 2006).

3. Incompleteness of data. For many organisms genetic data are absent or insufficient.

4. Ignoring other aspects. GSC does not take into account morphological, ecological, and evolutionary aspects that are important for understanding the biological essence of species.

Applicability in the agrosphere. GSC finds application in the diagnosis of pathogens, especially bacteria and viruses, where morphological characters are limited. For example, to identify species of Xanthomonas and Pseudomonas, methods of DNA-DNA hybridization and sequencing are used. In breeding, genetic markers make it possible to distinguish closely related species and lines, which is important for selecting resistance donors (Sigee, 1993; Agrios, 2005).

3.8. Other Species Concepts

Besides those listed, there are a number of other concepts, which we will consider briefly.

Cohesion species concept. Proposed by Alan Templeton (Templeton, 1989). A species is “the most inclusive group of organisms having the potential for phenotypic cohesion through intrinsic cohesion mechanisms.” Cohesion mechanisms include gene flow, genetic drift, and natural selection, which maintain the integrity of the species. This concept is applicable to both sexual and asexual organisms and allows limited gene exchange with other species.

Genealogical species concept. Proposed by Baum and Shaw (Baum & Shaw, 1995). A species is “a basal, exclusive group of organisms whose members are more closely related to each other than to any organism outside the group.” Exclusivity means that all alleles in the group have a common ancestor more recent than any ancestor outside the group. This concept works well with molecular data but requires a large amount of data and is inapplicable to organisms with horizontal gene transfer.

Differential fitness species concept. Proposed by Hausdorf (Hausdorf, 2011). A species is a group of organisms mutually characterized by characters that would have negative fitness consequences in other groups and that cannot be regularly transferred between groups. This concept emphasizes adaptive differences and allows gene exchange if it does not affect the characters determining differential fitness.

Ecological species concept (already considered above).

3.9. Comparison of Concepts and Their Applicability to Different Groups of Organisms

Different species concepts work differently for different groups of organisms. Table 3.1 compares the main concepts by criteria, applicability, and limitations.

Table 3.1. Comparison of the main species concepts

For plants, MSC (because of practicality) and PSC (taking molecular data into account) are most applicable. BSC is limited because of widespread hybridization and polyploidy. For cultivated plants, ecological and genetic concepts are also important, since cultivars and lines differ in ecological and genetic characters.

For fungi, MSC was long the main concept, but with the development of molecular methods PSC and GSC are acquiring increasing importance. BSC is applicable only to sexual forms, but many fungi reproduce asexually. For phytopathogenic fungi, ecological concepts (races, pathotypes) are also important.

For bacteria, BSC is inapplicable because of the absence of a sexual process. GSC (level of DNA similarity, ANI), PSC (phylogenetic trees based on concatenated genes), and the ecological concept are used. Horizontal gene transfer creates additional difficulties (Doolittle & Papke, 2006).

For animals, BSC was long dominant, especially for vertebrates. However, for invertebrates, especially insects with asexual reproduction, it is not always applicable. PSC and GSC are becoming increasingly widespread.

3.10. Significance for the Agrosphere: How the Choice of Concept Affects Practice

The choice of species concept has direct practical consequences for agronomy.

Diagnosis of diseases and pests. If an identification key is based on the morphological concept, it may not reveal cryptic species that differ in pathogenicity or resistance to pesticides. For example, the Gibberella fujikuroi complex includes 45 species, many of which differ in host range and toxigenicity; a morphological key will not allow distinguishing them (Taylor et al., 2000). For accurate diagnosis, molecular methods based on the phylogenetic or genetic concept are necessary.

Plant quarantine. Quarantine lists are compiled on the basis of taxonomic species. If a species is understood too broadly (for example, as a morphological species including several cryptic ones), quarantine measures may be insufficient. If too narrowly, unjustified prohibitions may result. Therefore, it is important that quarantine lists be based on modern taxonomic revisions taking molecular data into account.

Breeding for resistance. The search for resistance donors among wild relatives requires accurate species determination. If a wild relative is identified incorrectly, crossing may not give the expected result. In addition, understanding the structure of the pathogen species (presence of races, pathotypes) is necessary for creating resistant cultivars. For example, if the pathogen species is a complex of cryptic species, resistance to one species may not work against another.

Certification of seeds and planting material. Certification requires accurate identification of species, especially quarantine ones. An error in determination may lead to the spread of dangerous pathogens.

Biological control. Accurate determination of entomophages and antagonists is crucial for successful biological control. If a species is identified incorrectly, the released agent may fail to establish or may harm non-target organisms.

3.11. Chapter Summary

1. There are many species concepts reflecting the complexity of biological diversity. The main ones are: morphological, biological, phylogenetic, evolutionary, ecological, genetic, as well as the cohesion and genealogical concepts.

2. The morphological concept is the most practical and universal, but suffers from subjectivity and does not reveal cryptic species.

3. The biological concept emphasizes reproductive isolation but is inapplicable to asexual, prokaryotic, and hybridizing forms.

4. The phylogenetic concept requires monophyly and diagnosability; it works well with molecular data but may lead to species splitting.

5. The evolutionary concept defines species as a unique evolutionary lineage but is non-operational.

6. The ecological concept links species with an adaptive zone; it is important for understanding ecological races and pathotypes.

7. The genetic concept uses genetic distinctness; it is applicable to microorganisms but requires establishing thresholds.

8. For the agrosphere, the choice of concept has practical significance: diagnosis, quarantine, breeding, and biological control depend on it. The most practical approach is an integrative one, combining different criteria depending on the group of organisms and the tasks of the study.

4.1. Introduction: When Classical Ideas Fail

In previous chapters we examined the main species concepts and became convinced that none of them is universal. However, there exist groups of organisms and biological situations in which the application of any classical definition of species encounters fundamental difficulties. These “special cases” are not curiosities or exceptions—they are widespread in nature and directly relevant to the agrosphere, since they concern pathogens, pests, and cultivated plants (Stuessy, 2009; Zachos, 2018).

In this chapter we will consider five categories of such cases: cryptic species (sibling species); hybridization and introgression; polyploidy and apomixis; asexual organisms, prokaryotes, and viruses; horizontal gene transfer. Each of these cases requires a revision of habitual ideas about species and has important practical consequences for diagnosis, breeding, and plant protection.

4.2. Cryptic Species and Sibling Species

Definition and essence. Cryptic species, or sibling species, are genetically isolated, evolutionarily independent lineages that are morphologically practically indistinguishable. They do not correspond to the criterion of the morphological species concept but can be revealed using genetic, cytological, biochemical, or behavioral methods (Stuessy, 2009; Simpson, 2018).

The phenomenon of cryptic species is widespread in all groups of organisms. The causes of morphological similarity may be different: recent divergence of lineages (when morphological differences have not yet accumulated), stabilizing selection (when morphology is preserved while genetic and ecological differences accumulate), or convergence (when different lineages acquire a similar appearance under similar conditions) (Stuessy, 2009).

Examples in insects. A classic example from entomology is the complex Drosophila pseudoobscura and D. persimilis, morphologically almost indistinguishable but reproductively isolated. Another example is the grain moth (Tinea granella), which, as it turned out, represents a complex of four species, of which only two are harmful (Zakhvatkin, 2001). Among Coleoptera, sibling species have been found in the rice and granary weevils, which for a long time were considered one species Calandra oryzae. Sibling species have also been recorded in Orthoptera, ants, aphids, and springtails (Zakhvatkin, 2001).

For an agronomist, this means that identifying a pest “to species” on the basis of morphological characters alone may be insufficient. If two sibling species differ in resistance to an insecticide, in phenology, or in the spectrum of damaged crops, the control strategy must take this difference into account. However, to reveal it, additional methods are needed—genetic, biochemical, behavioral (Zakhvatkin, 2001).

Examples in fungi. In mycology, the problem of cryptic species is especially acute, since morphological characters of fungi are often limited and plastic (Taylor et al., 2000; Webster & Weber, 2007). A classic example is Armillaria mellea sensu lato (honey fungus), which represents a complex of more than a dozen species differing in biology, ecology, and pathogenicity (Taylor et al., 2000). Another example is Gibberella fujikuroi (teleomorph of Fusarium), in which molecular-phylogenetic methods revealed 45 species, of which 23 turned out to be new to science (O'Donnell et al., 1998; Taylor et al., 2000). Many of these species differ in the spectrum of affected crops and in the mycotoxins they produce.

An even more illustrative example is Histoplasma capsulatum, in which six genetically isolated groups have been revealed, correlating with geographic distribution and pathogenicity (Kasuga et al., 1999; Taylor et al., 2000). For phytopathology, an analogous situation is observed with Coccidioides immitis, in which two cryptic species have been revealed, differing in geographic distribution and physiological properties (Koufopanou et al., 1997; Taylor et al., 2000).

Examples in nematodes. Nematodes are another group in which cryptic species occur especially often. Root-knot nematodes (Meloidogyne spp.) represent a complex of species differing in the spectrum of affected crops and in resistance to nematicides. Identifying a nematode species solely by morphology may be insufficient for choosing a protection strategy (Stuessy, 2009).

Diagnosis of cryptic species. To reveal cryptic species, the following are used:

1. Molecular-genetic methods: DNA sequencing, microsatellite analysis, AFLP, RAPD, comparison of gene sequences (Taylor et al., 2000; Doolittle & Papke, 2006).

2. Cytogenetic methods: study of karyotypes, chromosomal rearrangements.

3. Biochemical methods: analysis of isoenzymes, secondary metabolites.

4. Ecological and behavioral methods: study of host range, phenology, mating behavior.

5. Crossing: testing reproductive isolation under laboratory conditions.

For an agronomist, the practical conclusion is this: if a morphological identification key does not give a satisfactory result, and the biology of the organism (pathogenicity, resistance to pesticides) does not correspond to the expected one, one should consider the possibility of a cryptic species and apply additional diagnostic methods (Sokirko, 2019; Taylor et al., 2000).

4.3. Hybridization and Introgression

Definition and essence. Hybridization is the crossing of organisms belonging to different species or taxa of higher rank. Introgression is the penetration of genes of one species into the gene pool of another through repeated backcrossing of hybrids with parental forms (Stuessy, 2009; Simpson, 2018).

In plants, hybridization is an extremely widespread phenomenon. According to estimates, about 25% of plant species participate in hybridization, and more than 70,000 natural interspecific hybrids have been described (Stuessy, 2009). Hybridization is especially characteristic of such groups as willows (Salix), oaks (Quercus), blackberries and raspberries (Rubus), hawthorns (Crataegus), irises (Iris), sunflowers (Helianthus), and many others (Stuessy, 2009; Judd, 2018).

Consequences of hybridization. Hybridization may have several consequences:

1. Strengthening of reproductive isolation. If hybrids are less fit than parental forms, natural selection may favor the development of stronger isolating barriers (Wallace effect).

2. Formation of hybrid swarms. With repeated crossings of hybrids with parents and among themselves, hybrid populations are formed that may exist for a long time.

3. Introgression. Genes of one species penetrate into the gene pool of another, which increases the genetic diversity of the latter.

4. Fusion of species. With intensive hybridization, two species may merge into one.

5. Origin of new species. Hybridization in combination with polyploidy may lead to the formation of new species (allopolyploidy).

Examples from the agrosphere. In cultivated plants, hybridization is widely used in breeding. For example, many modern cultivars of wheat, potato, tomato, rose, and other crops are the result of interspecific hybridization. Wild relatives of cultivated plants often serve as donors of genes for resistance to diseases and pests. However, hybridization may also have negative consequences: for example, during introgression of genes from genetically modified crops into wild populations or during “contamination” of the gene pool of cultivated plants by genes of wild relatives (Stuessy, 2009; Judd, 2018).

In pathogens, hybridization may lead to the appearance of new, more virulent races. For example, in fungi of the genus Phytophthora, hybridization between species may lead to the formation of new pathogens with an expanded host range (Agrios, 2005). In bacteria, horizontal gene transfer (see below) may play an analogous role.

Problem for systematics. Hybridization blurs boundaries between species. If two species interbreed and produce fertile offspring, then from the point of view of the biological concept they should be considered one species. However, in practice such species often retain their integrity despite limited gene flow. This creates difficulties for taxonomy: where should the boundary between species be drawn if they exchange genes? (Stuessy, 2009; Zachos, 2018).

For an agronomist it is important to understand that hybridization is not only a breeding technique but also a natural process that can influence the structure of pathogen and pest populations. For example, the emergence of new races of phytopathogens is often associated with hybridization or introgression (Agrios, 2005; Sokirko, 2019).

4.4. Polyploidy and Apomixis in Plants

Polyploidy. Polyploidy is an increase in the number of chromosome sets in a cell. A distinction is made between autopolyploidy (a multiple increase in the sets of one species) and allopolyploidy (the union of sets of different species, usually as a result of hybridization). Polyploidy is extremely widespread in plants: according to estimates, 30–40% of angiosperm species are polyploids, and among ferns up to 95% (Stuessy, 2009; Judd, 2018).

Polyploidy has important evolutionary and practical consequences. Polyploids are often larger, more resistant to unfavorable conditions, and more productive. Many cultivated plants are polyploids: wheat (hexaploid), potato (tetraploid), cotton (tetraploid), sugarcane (highly polyploid), banana (triploid), and others (Stuessy, 2009; Naida, 2021).

From the point of view of systematics, polyploidy creates a problem: a polyploid may be reproductively isolated from the parental diploid species but morphologically similar to them. In such cases the question arises: should the polyploid be considered a separate species? Modern systematics usually recognizes polyploids as independent species if they are reproductively isolated and have stable morphological or ecological differences (Stuessy, 2009; Soltis et al., 2007).

Apomixis. Apomixis is reproduction by seeds without fertilization. In apomixis, the embryo develops from an unfertilized egg cell (parthenogenesis) or from other cells of the ovule. Apomixis is widespread in angiosperms: it occurs in 34 families and 130 genera, especially often in Asteraceae, Poaceae, and Rosaceae (Stuessy, 2009; Simpson, 2018).

Apomixis creates serious problems for systematics, since in apomixis the offspring is genetically identical to the maternal plant, and recombination is absent. This leads to the formation of many small, weakly distinguishable “microspecies,” which are often regarded as separate species. For example, in the genus Taraxacum (dandelion) more than 2,000 species have been described, most of which are apomictic microspecies (Stuessy, 2009). In the genus Rubus (blackberry), the number of described species varies from 24 to 381 depending on the approach (Stuessy, 2009).

For an agronomist, apomixis has dual significance. On the one hand, apomictic crops (for example, some cultivars of blackberry, blackberry-raspberry hybrids) are convenient for propagation, since they preserve the properties of the maternal plant. On the other hand, apomixis complicates breeding, since it limits genetic recombination. In addition, apomictic complexes may include many microspecies differing in economically important characters (disease resistance, fruit quality), which requires careful diagnosis (Stuessy, 2009; Simpson, 2018).

Practical consequences. Polyploidy and apomixis are not “anomalies” but widespread and evolutionarily successful strategies of plants. For an agronomist it is important to understand that:

1. Many cultivated plants are polyploids, and their genetics differs from the genetics of diploids.

2. Apomictic complexes may include many microspecies differing in economically important characters.

3. In breeding, it is necessary to take into account the ploidy and mode of reproduction of the source material.

4.5. Asexual Organisms, Prokaryotes, and Viruses

Asexual organisms. Many organisms reproduce exclusively asexually: bacteria, some fungi, a number of plants and animals. For them the biological species concept is inapplicable, since interbreeding is absent. In such cases morphological, ecological, phylogenetic, or genetic concepts are used (Stuessy, 2009; Doolittle & Papke, 2006).

In asexual organisms, species boundaries are often determined on the basis of stable morphological, physiological, or ecological differences. However, with asexual reproduction, genetic variability may accumulate independently in different lineages, which leads to the formation of many clonal lines that are difficult to classify. For example, in apomictic plants (see above) the number of “species” may reach thousands (Stuessy, 2009).

Prokaryotes. Bacteria and archaea are a special group for which the concept of species is most problematic. Traditionally, bacterial species were distinguished on the basis of morphological, physiological, and biochemical characters. However, with the development of molecular methods it became clear that the genetic diversity of bacteria is enormous, and horizontal gene transfer makes boundaries between species blurred (Doolittle & Papke, 2006).

Modern approaches to defining bacterial species:

1. DNA-DNA hybridization: if the level of DNA similarity between two strains exceeds 70%, they are considered one species (Doolittle & Papke, 2006).

2. Average nucleotide identity (ANI): if ANI between two genomes exceeds 94–95%, they are considered one species (Konstantinidis & Tiedje, 2005; Doolittle & Papke, 2006).

3. Phylogenetic analysis: comparison of 16S rRNA sequences and concatenated sequences of conserved genes.

4. Ecological criterion: taking into account the ecological niche and physiological characteristics.

However, even these criteria do not always give an unambiguous answer. Horizontal gene transfer can lead to different parts of the genome having different evolutionary histories, and ecological and genetic boundaries between species may not coincide (Doolittle & Papke, 2006).

For phytopathology, the problem of species in bacteria has direct practical significance. For example, Pseudomonas syringae was long regarded as one species with many pathovars, but molecular studies showed that it is a complex of several genetically distinct groups (Sigee, 1993). Similarly, Xanthomonas campestris represents a complex of pathovars that differ in host range and pathogenicity. Accurate determination of the species of a bacterial pathogen is necessary for choosing a protection strategy and for quarantine measures (Sigee, 1993; Agrios, 2005).

Viruses. Viruses are a special category for which the concept of species is even more problematic. Viruses are not cellular organisms, they do not reproduce sexually, and their genomes are characterized by high rates of mutation and recombination (Van Regenmortel, 2010; Lauring & Andino, 2010).

The International Committee on Taxonomy of Viruses (ICTV) defines a virus species as “a polythetic class of viruses that constitutes a replicating lineage and occupies a particular ecological niche” (Pringle, 1991; Van Regenmortel, 2010). This definition reflects the cluster nature of species in viruses: a species is determined by a combination of characters (host range, antigenic properties, genome sequence), none of which is necessary and sufficient.

For an agronomist it is important to understand that viral species can change rapidly, and boundaries between them may be blurred. For example, strains of tobacco mosaic virus (TMV) may differ in symptoms and host range but remain within one species. On the other hand, different viruses may recombine, forming new pathogens (Van Regenmortel, 2010; Lauring & Andino, 2010).

Practical consequences. For asexual organisms, prokaryotes, and viruses, diagnosis is often based on molecular methods rather than morphology. This means that an agronomist must have access to appropriate laboratories or use commercial diagnostic kits. In addition, species names in these groups may be revised more often than in plants and animals, and this must be taken into account when working with databases and identification keys (Doolittle & Papke, 2006; Van Regenmortel, 2010).

4.6. Horizontal Gene Transfer in Bacteria and Its Influence on Phylogeny

Definition and essence. Horizontal gene transfer (HGT) is the transfer of genetic material between organisms that are not parents and offspring. In bacteria, HGT is carried out by three main mechanisms: transformation (uptake of free DNA from the environment), conjugation (transfer of DNA through a conjugation bridge), and transduction (transfer of DNA by bacteriophages) (Doolittle & Papke, 2006; Sigee, 1993).

HGT is widespread in bacteria and can occur even between organisms of different species, genera, and even domains. For example, antibiotic resistance genes are often transferred between different bacterial species, which leads to the rapid spread of resistance (Doolittle & Papke, 2006).

Influence on phylogeny. HGT creates serious problems for phylogenetics, since different genes in the genome may have different evolutionary histories. If HGT affects a significant part of the genome, then a phylogenetic tree built on the basis of one gene may not coincide with a tree built on the basis of another gene. This phenomenon is called “phylogenetic incongruence” (Doolittle & Papke, 2006; Zachos, 2018).

Moreover, HGT can lead to the genomes of different species becoming mosaic: some regions of the genome have a common origin with one species, others with another. In such cases, the concept of “species” as a reproductively isolated lineage loses meaning, since boundaries between species become blurred and dynamic (Doolittle & Papke, 2006).

Examples from the agrosphere. HGT is directly relevant to the agrosphere. For example, virulence genes in phytopathogenic bacteria are often localized on plasmids and can be transferred between different strains and species. This leads to the appearance of new, more virulent strains. Similarly, genes for resistance to antibiotics and bacteriocins can be transferred between bacteria, which complicates the control of bacterial plant diseases (Sigee, 1993; Agrios, 2005).

Another example is Agrobacterium tumefaciens, which transfers part of its plasmid DNA (T-DNA) into the plant genome, causing tumors (crown galls). This is a natural example of HGT between a bacterium and a plant (Sigee, 1993; Agrios, 2005).

The species problem in bacteria. HGT makes the species problem in bacteria especially complex. If different genes have different histories, which gene should be considered “determining” for the species? Modern approaches propose using concatenated sequences of conserved genes (“core genome”) for phylogenetic analysis, but even this does not always give an unambiguous result (Doolittle & Papke, 2006; Zachos, 2018).

Some researchers propose abandoning the concept of species in bacteria and using instead the concept of “genomic species” or “ecological species” (ecotype). Others propose using a “polyphasic” approach combining genetic, ecological, and phenotypic data (Doolittle & Papke, 2006; Rossello-Mora & Amann, 2001).

For an agronomist, the practical conclusion is this: when working with bacterial pathogens, it is necessary to take into account the possibility of HGT and, consequently, not rely exclusively on one genetic marker for identification. An integrated approach including phenotypic, ecological, and molecular data is more reliable (Sigee, 1993; Doolittle & Papke, 2006).

4.7. Why These Special Cases Are Important for the Agrosphere

All the special cases considered—cryptic species, hybridization, polyploidy, apomixis, asexual organisms, prokaryotes, viruses, HGT—are directly relevant to the agrosphere. They affect:

1. Diagnosis. An error in species determination may lead to the wrong choice of pesticide, the wrong protection strategy, or the spread of a quarantine organism.

2. Breeding. Understanding the structure of a pathogen species (presence of cryptic species, races, pathotypes) is necessary for creating resistant cultivars.

3. Quarantine. Quarantine lists must be based on modern taxonomic data taking into account the possibility of cryptic species and HGT.

4. Biological control. Accurate determination of the species of an entomophage or antagonist is necessary for successful biological control.

5. Certification. Certification of seeds and planting material requires accurate identification of species, especially quarantine ones.

4.8. Chapter Summary

1. Cryptic species (sibling species) are genetically isolated but morphologically indistinguishable lineages. They are widespread in insects, fungi, nematodes, and other organisms. To reveal them, molecular, cytogenetic, or biochemical methods are necessary.

2. Hybridization and introgression are widespread phenomena in plants and pathogens. They blur boundaries between species and may lead to the appearance of new, more virulent races.

3. Polyploidy and apomixis are widespread strategies of plants. Polyploids are often recognized as independent species if they are reproductively isolated. Apomixis leads to the formation of many microspecies, which complicates systematics.

4. Asexual organisms, prokaryotes, and viruses are groups for which the biological species concept is inapplicable. For them, morphological, ecological, phylogenetic, and genetic criteria are used.

5. Horizontal gene transfer in bacteria creates mosaic genomes and makes boundaries between species blurred. This is directly relevant to the evolution of pathogenicity and antibiotic resistance.

6. All these special cases are important for the agrosphere, since they affect diagnosis, breeding, quarantine, and biological control. Practical identification always requires critical thinking and an integrated approach.

5.1. Introduction: Why Confusion Arises

In practical work, an agronomist constantly encounters categories that designate groups of organisms but are not taxonomic species. Race, pathotype, biotype, strain, isolate—these terms are widely used in phytopathology. Cultivar, line, hybrid, cultivar—in plant growing. Breed, line, cross—in animal husbandry. All these categories share one thing: they describe groups of organisms but do not correspond to the taxonomic rank of species (Stuessy, 2009; Agrios, 2005).

Confusion between taxonomic and economically biological categories has not only terminological but also serious practical consequences. If an agronomist equates a pathogen race with a species, he may incorrectly choose a protection strategy. If a breeder confuses a cultivar with a species, he may incorrectly assess the genetic diversity of the source material. If a quarantine service includes an economic category instead of a taxonomic species in its lists, this leads to unjustified prohibitions or, conversely, to missing a dangerous organism (Zachos, 2018; Sokirko, 2019).

In this chapter we will examine the main agronomic categories, analyze their relation to taxonomic ranks, and show why they must be clearly distinguished. We will follow this logic: first we will consider categories of pathogens, then cultivated plants, then agricultural animals, and finally the key distinction between taxonomic rank and economically biological category.

5.2. Categories of Pathogens: Race, Pathotype, Biotype, Strain, Isolate

5.3. Categories of Cultivated Plants: Cultivar, Line, Hybrid, Cultivar

5.4. Categories of Agricultural Animals: Breed, Line, Cross

5.5. Key Distinction: Taxonomic Rank vs Economically Biological Category

All the categories considered—race, pathotype, biotype, strain, isolate, cultivar, line, hybrid, cultivar, breed, cross—share one thing: they are not taxonomic ranks. They are economically biological categories used for practical purposes—breeding, diagnosis, plant protection, animal husbandry (Stuessy, 2009; Zachos, 2018).

The key distinction between a taxonomic rank and an economically biological category is as follows:

1. Regulation. Taxonomic ranks are regulated by international codes of nomenclature (ICN for plants and fungi, ICZN for animals, ICNB for bacteria, ICTV for viruses). Economically biological categories are regulated by special codes (ICNCP for cultivated plants) or are not formally regulated (races, biotypes, strains) (Stuessy, 2009; ICNCP, 2016; Van Regenmortel, 2010).

2. Criteria of delimitation. Taxonomic species are delimited on the basis of evolutionary independence, reproductive isolation, or monophyly. Economically biological categories are delimited on the basis of economically important characters—virulence, productivity, resistance to diseases (Stuessy, 2009; Agrios, 2005).

3. Stability. Taxonomic names are more stable than economic ones. A species name may persist for decades; a race or strain name may change when new data appear (Zachos, 2018).

4. Universality. Taxonomic species are universal—they exist independently of practical needs. Economically biological categories are relative—they are distinguished for concrete purposes and may differ in different countries or for different crops (Stuessy, 2009).

5. Hierarchy. Taxonomic ranks form a hierarchy (species, genus, family). Economically biological categories do not form a formal hierarchy; they may intersect and combine (Stuessy, 2009; Pandey, 2021).

5.6. Why a Phytopathogen “Race” Is Not a Taxonomic Rank but Is Critically Important for Breeding for Resistance

5.7. Practical Consequences for Diagnosis, Breeding, and Quarantine

The distinction between taxonomic and economically biological categories has direct practical consequences for the agrosphere.

Diagnosis. In diagnosing diseases, it is necessary to distinguish the pathogen species (taxonomic category) from the race or pathotype (economic category). An error in species determination may lead to the wrong choice of protection strategy; an error in race determination—to the choice of the wrong cultivar. Accurate diagnosis requires both morphological and molecular methods (Agrios, 2005; Sokirko, 2019).

Breeding. In breeding for resistance, it is necessary to take into account both the taxonomic species of the pathogen and its racial composition. A cultivar resistant to one species may be susceptible to another; a cultivar resistant to one race may be susceptible to another. Breeders must work with race collections and use resistance genes effective against the maximum number of races (Agrios, 2005; Stuessy, 2009).

Quarantine. Quarantine lists should include taxonomic species, not economic categories. Including a race or strain in a quarantine list makes no sense, since a race may appear at any moment as a result of mutation. Quarantine measures should be aimed at preventing the introduction of a species, not its intraspecific variants (Zachos, 2018; Stuessy, 2009).

Certification. Certification of seeds and planting material should be based on taxonomic species, not economic categories. A cultivar may be certified by economic characters, but quarantine organisms must be identified to species (Stuessy, 2009).

Biological control. In biological control, accurate determination is necessary both of the target pathogen (to species and, where possible, to race) and of the biological control agent (to species). An error in determination may lead to ineffective biological control or to non-target effects (Stuessy, 2009).

5.8. Chapter Summary

1. In the agrosphere, categories are widely used that are not taxonomic species: race, pathotype, biotype, strain, isolate (in pathogens); cultivar, line, hybrid, cultivar (in cultivated plants); breed, line, cross (in agricultural animals).

2. Race is an intraspecific group of a pathogen differing in virulence to cultivars of the host plant. Race is not a taxonomic rank and is not regulated by ICN.

3. Pathotype is a group of strains with a certain spectrum of virulence; biotype is a group of strains with certain biochemical or physiological characters; strain is a pure culture of a microorganism; isolate is a culture isolated from a certain source.

4. Cultivar is an assemblage of cultivated plants distinguished by economically important characters and retaining them during propagation. Cultivar is not a taxonomic species; its name is regulated by ICNCP.

5. Line is a genetically uniform group of plants obtained by self-pollination or inbreeding. Hybrid is offspring from crossing genetically different forms. Cultivar is a synonym of cultivar in the broad sense.

6. Breed is an assemblage of agricultural animals of one species with common economically useful characters. Line and cross are categories of animal husbandry analogous to line and hybrid in plants.

7. Key distinction: taxonomic ranks are regulated by international codes of nomenclature and reflect evolutionary relationships; economically biological categories are regulated by special codes or are not formally regulated and reflect economically important characters.

8. A phytopathogen race is not a taxonomic rank but is critically important for breeding for resistance. The gene-for-gene concept explains why the appearance of new races leads to a “breakdown” of cultivar resistance.

9. For practical work it is necessary to clearly distinguish taxonomic species and economically biological categories. This is important for diagnosis, breeding, quarantine, certification, and biological control.

6.1. Introduction: Why Species Is a Hypothesis

In previous chapters we established that species is a central but problematic concept of biology. We examined many species concepts and became convinced that none of them is universal. We also analyzed special cases—cryptic species, hybridization, polyploidy, apomixis, asexual organisms, prokaryotes, viruses, horizontal gene transfer—which show that real biological diversity does not always fit into clear discrete categories. Finally, we distinguished taxonomic species and economically biological categories, which are often confused with species.

Now we have arrived at the key methodological position of modern systematics: species is a scientific hypothesis, not a fact (Stuessy, 2009; Zachos, 2018). This means that any delimitation of a species is an assumption about the boundaries of an evolutionarily independent lineage that can be confirmed, refined, or refuted as new data accumulate. Species is not a “given” that can simply be “discovered”; it is a model that the researcher builds on the basis of available data and that may be revised (Pavlinov, 2023; Simpson, 2018).

This position is of fundamental importance for the agrosphere. If species is a hypothesis, then species names may change, species boundaries may be revised, and different sources of information may give different answers to the question “What is this organism?” For an agronomist, this means the need for critical thinking and an understanding of which species concept a particular identification key or database uses (Zachos, 2018; Sokirko, 2019).

In this chapter we will consider three aspects of the problem: operationality (how species boundaries are tested); revision of species as data accumulate; consequences of name instability for practice.

6.2. Operationality: How Species Boundaries Are Tested

6.3. Revision of Species as Data Accumulate

6.4. Consequences: Instability of Names, Different Databases, Conflicts Between “Morphological” and “Molecular” Identification

6.5. How to Work with Species as a Hypothesis: Practical Recommendations

For an agronomist, practical recommendations for working with species as a hypothesis can be formulated as follows.

1. Use modern identification keys and databases. When identifying organisms, use current sources that take modern taxonomic data into account.

2. Check names against several sources. If a species name is doubtful, check it against several databases (NCBI, Mycobank, Index Fungorum, etc.).

3. Take the species concept into account. Understand which species concept a particular identification key or database uses. A morphological key may not reveal cryptic species; a molecular database may use the phylogenetic concept.

4. Apply an integrative approach. In identification, use several independent lines of evidence—morphological, genetic, ecological, cytogenetic.

5. Be prepared for revision. Species names may change as new data accumulate. Monitor taxonomic revisions, especially for groups important for the agrosphere (pathogens, pests, cultivated plants).

6. Consult specialists. In complex cases of identification, contact systematists and phytopathologists specializing in the relevant groups.

6.6. Chapter Summary

1. Species is a scientific hypothesis, not a fact. Any delimitation of a species is an assumption about the boundaries of an evolutionarily independent lineage that can be confirmed, refined, or refuted as new data accumulate.

2. Operationality means the possibility of testing the species hypothesis using available methods. The main criteria are morphological, genetic, ecological, and cytogenetic. Modern systematics uses an integrative approach combining several lines of evidence.

3. Species are revised as new data accumulate—molecular, ecological, cytogenetic, biochemical, biological. Examples: Gibberella fujikuroi (45 species instead of one), Histoplasma capsulatum (6 species), Coccidioides immitis (2 species), Armillaria mellea sensu lato (more than 10 species).

4. Consequences of species revision: instability of names, different databases, conflicts between morphological and molecular identification. This has direct practical consequences for diagnosis, quarantine, breeding, certification, and biological control.

5. For an agronomist it is important to understand that species is a hypothesis and to use modern sources, check names against several databases, take the species concept into account, and apply an integrative approach.

7.1. Introduction: Why It Is Important to Understand the Nature of Species

In previous chapters we established that species is not a static unit but a scientific hypothesis that may be revised as new data accumulate. We also showed that there are many species concepts, each with its own advantages and limitations, and that in the agrosphere economically biological categories (race, pathotype, cultivar, line) are widely used that are not taxonomic species (Stuessy, 2009; Zachos, 2018). Now we must answer the key question: what practical consequences does this have for agronomy?

The answer can be formulated briefly: understanding the nature of species directly affects the diagnosis of diseases and pests, quarantine measures, breeding for resistance, certification of seeds and planting material, and biological control. An error in species determination or a misunderstanding of what a species is can lead to serious economic and ecological consequences. In this chapter we will examine each of these areas in detail (Agrios, 2005; Sokirko, 2019).

7.2. Diagnosis of Diseases and Pests: An Error in Species Is an Error in Protection

7.3. Plant Quarantine: Which Species Are Prohibited and Which Are Not

7.4. Breeding: Searching for Resistance Donors Among Wild Relatives

7.5. Certification of Seeds and Planting Material

7.6. Biological Control: Accurate Determination of an Entomophage or Antagonist

7.7. Other Practical Consequences

Besides the areas listed, understanding the nature of species has other practical consequences for agronomy.

Biodiversity conservation. Understanding that species is a hypothesis is important for biodiversity conservation. If a species is split into several species, each of them may require separate conservation measures. If a species is merged, conservation measures may be revised (Zachos, 2018; Stuessy, 2009).

Ecological research. In ecological research, species are used as units of accounting. An error in species determination may lead to incorrect conclusions about community structure and ecological processes (Stuessy, 2009).

Education. Understanding that species is a hypothesis is important for education. Students should know that taxonomic names may change and that different sources may give different answers (Zachos, 2018).

International cooperation. Different countries may use different taxonomic concepts and different species names. This creates difficulties for international cooperation in quarantine, trade, and breeding (Zachos, 2018).

7.8. Chapter Summary

1. Understanding the nature of species has direct practical consequences for agronomy: diagnosis, quarantine, breeding, certification, and biological control.

2. Diagnosis: an error in species determination may lead to ineffective treatment, yield losses, and the spread of quarantine organisms. Cryptic species and races create special problems. An integrative approach using morphological, molecular, and ecological data is necessary.

3. Quarantine: quarantine lists must be based on modern taxonomic data. Cryptic species require molecular methods for detection. Races and pathotypes should not be included in quarantine lists as taxonomic species.

4. Breeding: the search for resistance donors requires accurate determination of the species of cultivated plants and their wild relatives, as well as pathogens. Cryptic species and races must be taken into account when creating resistant cultivars. Strategies include vertical and horizontal resistance, gene pyramiding, and multiline cultivars.

5. Certification: certification of seeds and planting material requires accurate identification of species. Cryptic species may create problems requiring molecular methods.

6. Biological control: accurate determination of the species of pests and biological control agents is necessary for success. Cryptic species may reduce the effectiveness of biological control.

7. For effective work, an agronomist must use modern sources, check names against several databases, take the species concept into account, and apply an integrative approach.

8.1. Species Is a Convenient but Not Absolute Unit

Throughout this lecture we have examined species from different sides: as the basic unit of biological diversity, as a scientific hypothesis, as the subject of many competing concepts, and as a category that in the agrosphere coexists with economically biological units. The main conclusion that follows from all of this can be formulated briefly: species is a convenient but not absolute unit (Stuessy, 2009; Zachos, 2018).

The convenience of species lies in the fact that it allows information about biological diversity to be “compressed” and made accessible for practical use. Without species it would be impossible either to construct a hierarchical classification, to organize diagnosis, or to conduct breeding work. Species is the level at which biological diversity becomes manageable and operational (Pavlinov, 2023; Simpson, 2018).

However, the absoluteness of species is an illusion. Species is neither an immutable essence nor a once-and-for-all given unit. It exists in space and time, changes in the course of evolution, and our ideas about its boundaries are refined and revised as new data accumulate. Cryptic species, hybridization, polyploidy, apomixis, horizontal gene transfer—all these phenomena show that boundaries between species may be blurred, and the concept of species itself requires refinement for different groups of organisms (Doolittle & Papke, 2006; Van Regenmortel, 2010; Zachos, 2018).

8.2. Species as a Hypothesis: What This Means for Practice

The key methodological position discussed in Chapter 6 is that species is a scientific hypothesis, not a fact (Stuessy, 2009; Zachos, 2018). This means that any delimitation of a species is an assumption about the boundaries of an evolutionarily independent lineage that can be confirmed, refined, or refuted as new data accumulate.

For practice this has several important consequences:

1. Species names may change. What yesterday was considered one species may today be divided into several, and vice versa. The pathogen name in an old identification key may not correspond to modern taxonomy (Sigee, 1993; Taylor et al., 2000).

2. Different sources may give different answers. Identification keys, databases, and molecular phylogenies may use different species concepts and, consequently, give different names for the same organisms (Zachos, 2018).

3. Practical identification requires critical thinking. An agronomist cannot simply “look in a key” and get a final answer. He must understand which species concept a given source uses, what limitations it has, and what additional methods may be required (Sokirko, 2019; Zachos, 2018).

8.3. What an Agronomist Should Remember

Summarizing, let us formulate several practical recommendations for an agronomist working with species in his professional activity.

First: distinguish taxonomic species and economically biological categories. Race, pathotype, biotype, strain, isolate are not taxonomic species but intraspecific or intrapopulation groupings. Cultivar, line, hybrid, cultivar are economic categories regulated by ICNCP, not ICN. Breed, cross are categories of animal husbandry. Confusing these levels leads to errors in diagnosis, breeding, and quarantine (Stuessy, 2009; Agrios, 2005; ICNCP, 2016).

Second: understand which species concept your identification key or database uses. A morphological key may not reveal cryptic species. A molecular database may use the phylogenetic concept, which leads to species splitting. A database based on the biological concept may merge species that do not interbreed in nature but are potentially capable of interbreeding (Zachos, 2018; Taylor et al., 2000).

Third: apply an integrative approach. Accurate identification requires combining morphological, molecular, ecological, and cytogenetic data. Do not rely on one character or one method (Stuessy, 2009; Simpson, 2018).

Fourth: monitor taxonomic revisions. Species names may be revised. This is especially true for pathogens and pests, for which molecular methods reveal more and more cryptic species (Taylor et al., 2000; O'Donnell et al., 1998).

Fifth: consult specialists. In complex cases of identification, contact systematists, phytopathologists, and ent