The species concept "problem" has pervaded for many years and will not be resolved anytime soon, if ever. The problem, of course, being that no two scientists will agree on universal definitions of what the darn things are! Taxonomist are exceptional argumentative and someone will undoubtedly disagree with everything in this article!
Species concepts were first defined based on morphological traits. Linneaus, being limited by technology at the time, used the "eyeball method" to study things - meaning he looked at them and described what he saw. This is formalized as the morphological or typological species concept (Cracraft, 2000; Mayr, 1996), and many biologists are just fine with this. It looks different, ergo it is and any distinguishing characters that could be observed, counted and measured were enough to define new species.
Characters are delimited by the practicing taxonomist and thus not all-inclusive of the whole organism. Morphological characters are typically those most easily observed, although the level of observation (i.e. from external features to cellular features) can have large effects on species identification and definition. For instance, Winston (1999) describes a case where closer observation of a western Atlantic species of the hermit crab hitch-hiking hydroid Hydractinia echinata, typically found off the coasts of Europe, resulted in the description of two additional species based on previously “hidden”, or non-scrutinized, morphological and ecological characters (Buss and Yund, 1989). Similar case are all too common. The closer we peer, the more we find.
The typological species concept idealized a species into an individual that represented a character or suite of characters that differentiated it from all other individuals. Thus, followers of this concept were forced to ignore population level variation. This plasticity of traits causes confusion and obscures the nature of a species particular adaptations. An extreme, but really fascinating, example comes from deep-sea hydrothermal vents off the coast of the Pacific northwest. A large polychaete tubeworm, Ridgeia piscesae, was originally described as two species due to two very unique morphotypes (see image below). Hydrothermal vent tubeworms are known to harbor symbiotic bacteria which use hydrogen sulfide as a chemical energy source, which is readily abundant coming out of the vents.
[caption id="attachment_515" align="aligncenter" width="542" caption="Ridgeia piscesae, from Carney et al. 2007. a) generalized body form, b) short-fat morphotype, c) long-skinny morphotype."][/caption]
Despite living within a stone throw of each other, populations of the "short-fat" and "long-skinny" tubeworm have completely different phenotypes. It was a few years later that with a suite of nuclear and mitochondrial genetic markers that it was realized that the two morphotypes were genetically indistinguishable. This phenotypic plasticity is the result of differential gene expression related to which environment the larvae settle in (Carney et al. 2007): active black smoker chimneys, which are characterized by higher hydrothermal flow, higher temperatures and greater sulfide concentrations or diffuse-flow hydrothermal fields. Even though the morphology is so different they were combined into one species.
Mayr (1942) brought the species concept from the individual level to the population level by defining species as discrete populations of individuals that are reproductively isolated, or unable to. A problem with this view of species is that data on inter-breeding are typically not known and museum specimens are often collected with disregard to such data (Wheeler, 1999). Mallet (1995) even went so as to call reproductive isolation a useless concept because it cannot be tested. Others have countered that all species concepts are inherently untestable by experimentation or observation (Coyne and Orr, 2004). Claims of biological species are often typological species in practice.
Mallet (1995) defined the genotypic cluster species concept to refute some of the pitfalls of the biological species concept and incorporate additional knowledge from genetics in terms of ‘identifiable genotypic clusters’ with no appreciable heterozygotes. Coyne and Orr (2004) argued that the genotypic clustering species concept focuses on identification of species and not the origin of species, is not conservative enough, and will over-recognize species in sympatry compared to the biological species concept. Furthermore, they argue that since the genotypic clustering concept is non-hierarchical, it doesn’t reflect the hierarchical nature of evolution and confuses polymorphic forms and Batesian mimics without introducing a reproductive criterion (Coyne and Orr, 2004).
While the biological species concept emphasizes isolating mechanisms which separate members of a species, the recognition (Patterson, 1985) and cohesion (Templeton, 1989) species concepts emphasize keeping members of a species cluster intact. The recognition species concept focuses on a shared fertilization system between individuals. Thus, it can only consider barriers to fertilization as modes of speciation. Coyne et al. (1988) considered this to be a subset of the biological species concept. Templeton (1989), on the other hand, contended that the advantage of the cohesion species concept was its emphasis on mechanisms that enforced gene flow between populations. This made it superior to the biological species concept in dealing with asexual and hybridized sympatric clusters that maintained their identities. Harrison (1998) brought a particular valid criticism to the approach of cohesion: “... life cycles and habitat associations have not been molded by selection for the purpose of ‘cohesion’.” (pg. 25). That is to say that selection appears to be a non-cohesive force by definition.
There are other concepts as well, Mayden (1997) lists 22-24 different conceptualizations and philosopher of science John Wilkins* lists 26. The above concepts view the species as the end-point of evolution, without considering the historical nature of the process of evolution. Hennig (1966) recognized this fact and argued for a temporal component to systematic theory which he termed phylogenetic systematics. Though many subsequent authors agree with Hennig in the use of a phylogenetic concept of species, several authors disagree on the particulars. This has led to differences in interpretation of what a species is and how species are related to one another. The Hennigian species concept incorporated the interbreeding model of a biological species concept, but with a historical component. This was modified by Willmann (1986) to specifically state that species are reproductively isolated and originate via a stem species branching off into two new species. The stem species, by definition, ceases to exist by way of either extinction of speciation. The latter point is important to proponents of this species concept because with dissolution of the stem species, monophyly (a species and all of its descendants) can be maintained.
Other authors have other interpretations of what a phylogenetic species concept is. The main concepts differ between whether species are viewed as irreducible clusters that are diagnostically distinct from other clusters (Wheeler and Nixon, 1990), as exclusive monophyletic units (de Queiroz and Donoghue, 1988), or as a group of organisms whose genes have more recently coalesced with each other relative to organisms outside that group and containing no exclusive group within it (Baum and Donoghue, 1995). At first glance, the species concept proposed by Baum and Donoghue (1995) appears to most accurately reflect evolutionary history. Upon closer inspection, it is nearly impossible to have complete knowledge of the evolutionary history of all genes in all the organisms in an analysis.
In practice, purveyors or this species concept have often used one or a few loci in delimiting species (Coyne and Orr, 2004). Shaw (2001) relaxed this extreme assumption to “greater than 50%”, meaning that a species is delimited if most of the genes have coalesced. While operationally useful, this definition may be just as arbitrary as using diagnostic morphological characters. Describing species as exclusive monophyletic units seeks to overcome such arbitrariness and potentially has the greatest power of all species concepts discussed here to represent a true phylogeny. But it is known that phylogenies based upon genes do not necessary reflect a species true phylogeny, which may never be known with certainty (Avise and Wollenberg, 1997).
Proponents of the evolutionary species concept claim theirs can be mos universally applied relative to all others. Wiley (1978) purported that a species concept must satisfy five criteria: universal validity, allow for testable hypotheses, include valid special case species definitions, specify what types of species origins are possible or not possible, and be “capable of dealing with species as spatial, temporal, genetic, epigenetic, ecological, physiological, phenetic, and behavioral entities” (pg. 18). Modifying an earlier concept from Simpson (1961), Wiley states: “A species is a single lineage of ancestral descendant populations of organisms which maintains its identity from other such lineages and which has its own evolutionary tendencies and historical fate.” Wiley’s modification removed the need for species to be changing, as originally defined by Simpson (1961). The criticisms levied against the evolutionary species concept appear to be more about lack of operational criteria to delimit species spatio-temporally (Wheeler and Meier, 2000).
An additional outcome of the species concept debate is the view that only populations are real and that species are artifacts (Brooks and McLennan, 1999). Darwin (1859) believed that species were arbitrary constructs of the taxonomist for convenience, while Mayr believed that species were real entities (Mayr, 1996). Levin (1979) championed the view that species are the empirical units of evolution and ecology, while evolutionary species concept supporters argued that if monophyletic groups are real then so are species (Wiley and Mayden, 2000b). Other interpretations span the range between arbitrary constructs and representing real natural entities. Furthermore, it seems as if every taxonomist is trying to find that one perfect species concept that works for all scenarios and types of organisms (Hey, 2001; Hey, 2006; Wheeler and Meier, 2000).
Several authors have advocated for pluralism, or the use of multiple species concepts (Mayden, 1997; Mayden, 1999). Different situations or questions may call for using different species concepts. Hey (2006) cautions against this though, stating it doesn’t help to settle anything regarding the species debate. Fitzhugh (2006) treads close to a pluralistic view species in his advocacy for a "requirement of total evidence" approach to systematics. This requirement suggests that any evidence relevant to the species question needs to be considered. Total evidence could include morphological character information, genetic characters, behavioral traits and more. While perhaps not setting out to satisfy multiple species concepts, the requirement for total evidence may do just that along the way.
As with many biologists studying biodiversity and other taxonomists, I feel unsatisfied by the current plethora of species concepts. Those attempting to be generally applied, such as the phylogenetic, Hennigian and evolutionary species concepts, tend to inflate biodiversity by elevating subspecies, or perhaps even distinct populations to species status. I’m unsure whether this inflation is due to the flexibility in the definitions, viewing species as lineages or clusters, or the taxonomic practice of the practitioners.
Those attempting to restrict the definition or discount evolutionary processes, like the biological species concept, tend to underestimate biodiversity. Additionally, the biological, recognition and cohesive species concepts cannot satisfactorily deal with asexual organisms and are unable to be applied broadly within only the animal kingdom. While reproductive isolation may be an important criterion for speciation to occur, other mechanisms are known such as hybridization, recombination, horizontal gene transfer (can occur between a eukaryote and prokaryote as shown in recent research: see Hotopp et al., 2007) to name but a few. Reproductive isolation may also be a product of speciation and not a causal mechanism (Mishler and Donoghue, 1982; Wiley and Mayden, 2000a).
As do the proponents of the evolutionary species concepts, I believe that species are real, are individuals and ancestral species do not need to become extinct during a speciation event. I view the act of formally describing a species as formulating a hypothesis about that species' unique suite of characters and the evolutionary history of the retention, loss or modification of those characters over time. I believe the evolutionary species comes closest to my views of what species are. I agree that species are entities of organisms that maintain its identity throughout time and space from other entities. This is a key factor to species being operationally and pragmatically useful. I understand this might not sit well with philosophers and some other evolutionary biologists. Some of the phylogenetic species concepts recognize too many species, whereas some of reproductive isolationist concepts ignore asexual and allopatric species. The latter is unacceptable and the former may give a misleading foundation for other areas of study (i.e. biodiversity ecology) to test hypotheses on.
* Though I haven't read the book, John Wilkins is an authority on species concepts and recently published Species: A History of an Idea, which promises to be informative and interesting!
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