LINEAGE-BASED SPECIES CONCEPTS
To understand lineage-based species concepts, the terms “lineage” and “population” have to be defined at first. A lineage is defined as “an ancestral–descendant sequence of populations” (Simpson 1961). The term population is usually defined as a group of conspecific organisms that occupy a more or less well-defined geographical region and exhibit reproductive continuity from generation to generation (Futuyma 1998). There are several variations of this definition (Waples and Gaggiotti 2006). In any case it has to be specified which of the individuals that co-occur in an area form a population. In some definitions of “population” the more usual phrases “conspecific organisms” or “individuals of the same species” are replaced by “interbreeding individuals” (e.g., Mayr 1942, 1963; de Queiroz and Donoghue 1988). However, such a definition of population introduces the biological species concept through the back-door by including it into the definition of population. This definition was not used by de Queiroz (1998) when he introduced the general lineage concept. Rather, he emphasized that he uses population “in the general sense of an organizational level above that of the organism rather than the specific sense of a reproductive community of sexual organisms” (de Queiroz 1998). He did not specify any properties of this “organizational level above that of the organism,” leaving the exact definition of population and, thus, lineage and species unclear. The later addition of the term metapopulation to the general lineage concept and its definition as “an inclusive population made up of a set of connected subpopulations” by de Queiroz (2005a,b) did not help to clarify the concept, rather introduced additional undefined terms. It has neither been explained how “subpopulations” are defined nor how they are “connected.”
If the usual definition of population as a group of conspecific organisms that occupy a more or less well-defined geographical region is accepted, a population (and hence, a sub- or a metapopulation) can only be delimited if we can decide which organisms are conspecific. Thus, species must be defined before populations can be delimited. It is circular to define a species as a sequence of (meta-)populations, because it is part of the definition of “population” that the organisms that form a population belong to the same species. The term “population” must not be used in definitions of “species” unless it is defined without referring to conspecific organisms. Note, that this is necessary to avoid circularity and does not indicate any doubts about the evolutionary importance of populations.
The notion of “separately evolving” units is doubtlessly the core of all modern species concepts. However, to be a useful criterion in a species concept, it has to be specified what “separately evolving” means. It is unclear how populations connected by limited gene flow should be classified. As a result of introgression, biparental taxa may not evolve separately at some loci, but do at most others (Harrison 1998; Wu 2001; Coyne and Orr 2004; Wu and Ting 2004; Mallet 2005). Moreover, coherent polyphyletic entities that originated by parallel speciation and evolve separately of the ancestral species cannot be classified as separate species by lineage-based species concepts.
Lineage-based species concepts shift the problem of defining the term “species” to the problem of defining the term “population” and result in an intricate re-formulization of the biological species concept or in circular reasoning. Furthermore, the important criterion “separately evolving” in the general lineage concept remained unclear, because it was not specified what this notion means. Thus, lineage-based species concepts present only limited progress toward a generally applicable species concept.
BIOLOGICAL SPECIES CONCEPT
The most influential species concept is still the biological species concept that defines species as “groups of actually or potentially interbreeding natural populations, which are reproductively isolated from other such groups” (Mayr 1942, 1963; “natural populations” in this formulation can be replaced by “individuals” without change of meaning). However, two of the new findings challenge the biological species concept. The finding that reproductive barriers are semipermeable to gene flow and that species can differentiate despite ongoing interbreeding (Harrisson 1998; Rieseberg 2001; Wu 2001; Rieseberg et al. 2003; Coyne and Orr 2004; Wu and Ting 2004; Mallet 2005, 2008; Lexer and Widmer 2008) indicates that the biological species concept is not in accordance with current use of the term species. Acceptance of this concept would require lumping many well differentiated and generally accepted species that nevertheless interbreed regularly. Some authors (Orr 2001; Noor 2002; Coyne and Orr 2004) have argued for a relaxed interpretation of the biological species concept to retain it despite the new insights. However, the meaning of a species concept is that it defines the conditions under which a group of individuals should be classified as a species. If we ignore the conditions specified in a species concept, it becomes useless.
Moreover, the biological species concept has originally been formulated exclusively for biparental organisms. Acceptance of the biological species concept would entail that the term species should not be used for uniparental organisms, although growing evidence indicates that they are organised in units that resemble species of biparental organisms (Holman 1987; Gevers et al. 2005; Cohan and Perry 2007; Fontaneto et al. 2007; Cohan and Koeppel 2008). It has been suggested that a modification of the biological species concept can be applied to uniparental prokaryotes (Dykhuizen and Green 1991). This was based on the insight that prokaryotes are not simple clonal organisms, but that there is frequent gene exchange at least in some groups. However, gene exchange between prokaryotes is not limited to closely related species (Ochman et al. 2005) and, thus, an application of a modification of the biological species concept would require lumping many well-differentiated and generally accepted species. Furthermore, there are uniparental organisms without gene exchange such as parthenogenetic species, for which even a modification of the biological species concept would not be applicable.
PHYLOGENETIC SPECIES CONCEPT
One important alternative to the biological species concept that can principally be applied also to uniparental organisms is the phylogenetic species concept. According to the diagnosable version of the phylogenetic species concept, a species is “a diagnosable cluster of individuals within which there is a parental pattern of ancestry and descent, beyond which there is not, and which exhibits a pattern of phylogenetic ancestry and descendent among units of like kind” (Eldredge and Cracraft 1980). This concept has also been recommended for prokaryotes (Staley 2006) and has recently been referred to in several DNA barcoding/DNA taxonomy studies (e.g., Kelly et al. 2007; Sarkar et al. 2008; Monaghan et al. 2009).
However, there are problems with this concept in uni- as well as in biparentals. In uniparentals in which there is no or little gene exchange, each clone with a mutation would be classified as a separate species (Coyne and Orr 2004). In uniparentals with higher levels of gene exchange and in biparentals each substitution will have its own particular distribution and little or no concordance might exist among the sets of individuals diagnosable with independently derived mutations except those bounded by barriers to gene flow (Avise and Ball 1990). Eldredge and Cracraft (1980) restricted the clusters of individuals that are ranked as “species” by including the condition “within which there is a parental pattern of ancestry and descent, beyond which there is not” in the concept. This condition has the function to restrict the cluster of individuals that are ranked as “species” to those that are bounded by barriers to gene flow. However, the insights that hybridization between closely related species is frequent and that species can differentiate despite ongoing interbreeding means that many currently recognized species do not show separate “parental patterns of ancestry and descent,” but that some descendants belonging to one species may have ancestors belonging to another simultaneously existing species and vice versa. Thus, these insights have similar consequences for the application of the phylogenetic species concept as for the biological species concept. Acceptance of the phylogenetic species concept would also require lumping many well-differentiated and generally accepted species that nevertheless interbreed regularly.
Moreover, polyphyletic species originating by parallel speciation will also not show a “parental patterns of ancestry and descent” separate from that of the ancestral species and would have to be lumped under the phylogenetic species concept, too.
GENOTYPIC CLUSTER DEFINITION
Mallet (1995) recognized that the biological species concept is untenable in the face of gene flow between independently evolving units and proposed a pattern-based species concept. Adding genetics to the phenetic species concept that defines species as groups of individuals with few or no intermediates, he formulated the genotypic cluster definition according to which a species is a “genotypic cluster that can overlap without fusing with its sibling.”
Just as the phylogenetic species concept, this concept is in principle applicable also for uniparental organisms. However, acceptance of the genotypic cluster definition would result in the undesirable consequence that each genetically different clone will be identified as a separate species (Coyne and Orr 2004).
The prediction that species sooner or later form genotypic and phenotypic clusters can be derived from most species concepts. Thus, this is doubtlessly a useful criterion for delimiting provisional species. However, incipient species might not yet be recognizable as distinct clusters based on a random sample of genetic markers. In the case of peripatric speciation, the peripheral species will initially often form a cluster with neighboring populations of the more widespread species so that the more widespread species does not form a genotypic cluster distinct from the peripheral species. At least in their initial stages, coherent entities originating by parallel speciation from different populations of an ancestral species cannot be recognized as separate genotypic clusters and would have to be lumped with the ancestral species under the genotypic cluster definition.
COHESION SPECIES CONCEPT
Templeton (1989) recognized that there is a whole continuum of reproductive systems from uni- to biparentals and that any a priori restriction of the scope of a species concept with regard to reproduction mode is to some degree artificial. Furthermore, he recognized that evolutionary processes other than reproductive isolation contribute also to the formation and maintenance of coherent entities, especially in uniparentals. Templeton (1989) compiled these processes and classified these “cohesion mechanisms” into mechanisms affecting genetic exchangeability by defining the limits of spread of new genetic variants through gene flow and mechanisms affecting demographic exchangeability by defining the fundamental niche and the limits of spread of new genetic variants through genetic drift and natural selection. However, the term “cohesion mechanism” may be misleading, because most biological properties that confer cohesion did probably not arise for that purpose (Harrison 1998). Thus, cohesion is an effect, not a mechanism. Based on the “cohesion mechanisms,”Templeton (1989) formulated the cohesion species concept, according to which a species is “the most inclusive group of organisms having the potential for genetic and/or demographic exchangeability.”
Coyne and Orr (2004) claimed that the cohesion species concept may fail to provide a decision about the species status of two groups when the criteria of genetic and demographic exchangeability conflict, for example, if two groups of biparental individuals are genetically nonexchangeable but demographically exchangeable. This is not the case. The “and/or” between genetic and demographic exchangeability in Templeton's (1989) formulation of the cohesion concept is a logical “or,” an inclusive disjunction. Thus, all individuals connected by any “cohesion mechanism” are classified as one species by the cohesion concept. If there are, for example, groups of biparental individuals that are genetically nonexchangeable (i.e., reproductively isolated), but demographically exchangeable, the most inclusive group includes all individuals. Thus, groups of individuals would have to be considered conspecific under the cohesion concept, if they occupy the same fundamental niche, even if they are reproductively isolated. Acceptance of the cohesion concept would require lumping many generally accepted reproductively isolated species. Moreover, the cohesion concept does not specify which kind of gene flow affects genetic exchangeability and, thus, will also result in lumping species that differentiate despite ongoing gene exchange.
GENIC SPECIES CONCEPT
Wu (2001) developed a novel model of speciation based on a consideration of the genetic processes happening during speciation, which explains why and what kind of gene exchange does not affect the persistence of differentiated species and the further differentiation of species. According to this model, the whole process of speciation depends primarily on the genes responsible for differential adaptation to different natural or sexual environments, the “speciation genes” (see also Wu and Ting 2004). Wu (2001) defined differential adaptation as a form of divergence in which the alternative alleles of a gene have opposite fitness effects in two groups of individuals. During the process of speciation the speciation genes may account for only a small fraction of the genome. Gene exchange is restricted at these loci, whereas gene exchange at other loci, the “marker loci,” could persist for a long period of time even after speciation. Speciation is the stage where the groups of individuals will not lose their divergence upon contact and will be able to continue to diverge. Based on this model, Wu (2001) defined species as “groups that are differentially adapted and, upon contact, are not able to share genes controlling these adaptive characters, by direct exchanges or through intermediate hybrid populations.” Although it was originally formulated for biparental species, this concept is in principle also applicable to uniparentals.
The genic species concept of Wu (2001) has been criticized because it exclusively focuses on differential adaptation caused by mutations in genes (Britton-Davidian 2001; Orr 2001; Rundle et al. 2001; Noor 2002). Other genetic features that may result in reproductive isolation such as chromosomal changes were classified as “special cases” by Wu (2001). However, the critics prefer to classify entities that evolve separately because they are reproductively isolated due to chromosomal changes or other nongenic mutations as separate species. Even if differential adaptation would be the most frequent process resulting in speciation, other processes that might also cause the formation of species such as genetic drift should not be excluded a priori in a species concept (Britton-Davidian 2001; Orr 2001; Rundle et al. 2001; Noor 2002).
DIFFERENTIAL FITNESS SPECIES CONCEPT
Compared to other species concepts, the ability of the genic species concept of Wu (2001) to specify in which cases groups of individuals can be classified as species despite gene flow between these groups represented an important conceptual advance. Thus, it is worth considering whether the two criticized restrictions of the genic species concept, that it considers only species that originated by (1) mutations in genes resulting in (2) differential adaptation, can be abolished. Wu (2001) defined differential adaptation by “opposite fitness effects” of alternative alleles. However, the features that cause speciation do not necessarily have to be alternative alleles and their fitness effects do not necessarily have to be opposite in different species, that is positive in the species that they characterize and negative in the other species. To restrict gene flow, it is sufficient that such features, which may be heritable traits other than genes, have negative fitness effects in other species. They may be neutral in the species that they characterize. For example, a Wolbachia infection may be nearly neutral in the hosting species but would have a negative fitness effect in other, noninfected species. Groups of individuals become evolutionary independent only if gene flow is restricted in both directions. Thus, each group must have features that have negative fitness effects in the other species. Based on these ideas, species can be defined as groups of individuals that are reciprocally characterized by features that would have negative fitness effects in other groups and that cannot be regularly exchanged between groups upon contact.
This differential fitness species concept considers not only mutations in genes, but any differences including, for example, chromosomal changes (White 1954; Rieseberg 2001), Wolbachia infections (Hurst and Schilthuizen 1998; Telschow et al. 2005; Werren et al. 2008), other selfish genetic elements such as transposable elements (Hurst and Schilthuizen 1998; Hurst and Werren 2001) or niche-specifying genes or sets of genes acquired by horizontal transfer in prokaryotes (Ochman et al. 2005; Cohan and Koeppel 2008). The differences may result from differential adaptation due to natural or sexual selection, but may also be the result of genetic drift or other often nonadaptive processes such as polyploidization or infections by symbionts. The features may be specifically adaptive for one group's niche, but maladaptive for another's or may be incompatible in the context of the genetic background of another group (like different Wolbachia infections). Such incompatibilities could result in lowered fertility or in unbalanced physiological function. As the genic species concept, the differential fitness concept allows for the exchange of genes as far as they are not important for the features that have negative fitness effects in the other species.
The differential fitness species concept differs from the biological species concept in considering that the exchange of the species-specific features may not only be restricted by reproductive isolation, but also by divergent selection. In this respect, the differential fitness species concept is closer to Darwin's (1859) understanding of species than to the biological species concept. Darwin (1859: 485) argued “that the only distinction between species and well-marked varieties is, that the latter are known, or believed, to be connected at the present day by intermediate gradations, whereas species were formerly thus connected.” The lack of intermediate gradations in the first differences that characterize nascent species results from the inability to exchange these features between groups and is not necessarily connected with reproductive isolation. One shortcoming of a purely phenotypic assessment of the ability to exchange potentially species-specific features is that groups of individuals characterized by different discrete polymorphisms may be taken for separate species because of the lack of intermediate gradations. However, this does not affect the differential fitness species concept that does not focus on the lack of intermediate gradations as such, but is based on the inability to exchange species-specific features between groups. As long as groups of individuals characterized by different discrete polymorphisms are able to exchange these polymorphisms, that is the underlying genes, these groups are not considered species under the differential fitness species concept. But when this ability disappears, groups of individuals characterized by different features become species under this concept.
The differential fitness species concept can be applied to the whole spectrum of organisms from uni- to biparentals. The differential fitness species concept classifies groups as species if they are characterized by features that would have negative fitness effects in other such groups and that cannot be regularly exchanged between these groups. In biparentals these features include besides adaptations to different environments also modifications of the reproductive system that decide with which other individuals an individual can produce fertile descendants. For example, polyploidy has a negative fitness effect in a group of diploid individuals, because it would result in reproductive incompatibility. Likewise, diploidy has a negative fitness effect in a group of polyploid individuals. Thus, these groups are classified as different species under the differential fitness concept, even if they occupy the same niche. Uniparental groups characterized by features that would have negative fitness effects in other groups occupy different niches in most cases. Thus, in uniparentals species as defined by the differential fitness concept correspond usually to ecotypes, which were actually considered the equivalent of biparental species in prokaryotes (Gevers et al. 2005; Cohan and Perry 2007; Cohan and Koeppel 2008). However, mutations in different genes in different strains, each of which is selectively neutral on its own, might result in genic incompatibilities, that is, might have negative fitness effects in strains with incompatible mutations in other genes, so that such strains qualify as different species under the differential fitness concept, even if they are not ecologically differentiated. It is questionable whether neutral mutations often persist long enough in prokaryotes that such genic incompatibilities can arise or whether they are usually eliminated by periodic selection before genic incompatibilities can originate.