The unnatural concept of “species”

It would seem unwise to look into the diversity without introducing its most fundamental and universal unit: the species. Althought the “species” concept has been and is still widely used in science and numerous other fields, it appears impossible to define it in a way that applies to all organisms. And this to such an extent, that many biologists simply stopped believing in the existence of the species as a taxonomic level, i.e. category. Among them Darwin, who dedicated a great part of his work to this term but still considered it as indefinable.

« It is really laughable to see what different ideas are prominent in various naturalists' minds, when they speak of ‘species’; in some, resemblance is everything and descent of little weight

— in some, resemblance seems to go for nothing, and Creation the reigning idea — in some, sterility an unfailing test, with others it is not worth a farthing. It all comes, I believe, from trying to define the indefinable. » (Darwin, 1887).

It may be useful to start with the prior definition of the word “species”, namely its etymologic root. From Latin “speciō” meaning “see” and “speciēs” meaning “appearance”, the term “species” contains intrinsically the idea of “showing some traits”. Thus, a first definition of “species” could be “a set of organisms showing common traits specific to them”.

This definition fits to the essentialist point of view, prevailing from Aristotle to Linnaeus and describing species as “natural kinds with eternal essences”. Each and every member of a kind is sharing a common essence which is, at the same time, responsible for the traits typically associated with those members. However, this definition induces two problems. The first one is that biologists sometime failed to find traits occurring in all members of a species and the second one is that they often also failed to find traits occurring exclusively in the members of a species.

Natural environment does not produce exact replicates but rather displays phenotypic diversity. Actually, each of the traits which constitute a species according to the essentialist definition could eventually disappear in the offspring. To conserve this definition, only the traits which will pass to the next generations (genetically inherited) should thus be considered.

Therefore, an improved definition for “species” could be “a set of organisms sharing traits which will all be transmitted to the offspring”. However, environmental parameters alone decide which traits will be, by the way of selection, transmitted. Since those parameters can not be totally predicted, one could define the species category but would fail to describe any of them.

The second problem related to the essentialist definition of species is also induced by the natural selection process. According to the definition, a trait defining a species should be unique to that species. There are numerous examples of extremely specific traits shared by asunder species. This phenomenon results from a convergent evolution creating similarities coming from independent origins (homoplasy). For instance, there are striking morphological likenesses between the shell of bivalves and that of brachiopods, however not closely related;

between the spiny stems of Euphorbiaceae and Cactaceae; between river dolphins Iniidae and Platanistidae; or even, between cuttlefish and mammalian eyes. Convergent evolutions also occur at molecular level, like for the antifreeze glycoproteins in Antarctic notothenioid fish and Arctic cods (Chen et al., 1997) and the amino acid sequence convergence of the lysozyme from the stomach of cows and colobine monkeys (Stewart et al., 1987). In each case the same evolutionary answer is proposed to an ecological problem. At first sight, it should be a quite unlikely mechanism because phenotypic differences are supposed to be controlled by many genes. The probability that the entire set of genes implied in one phenotypic trait evolves to produce the same result than for a different and independent organism should be thus very low. However, some investigations show a totally different situation. Firstly, many quantitative traits would be actually controlled by few genes, increasing the probability of a convergent evolution (Tanksley, 1993). Secondly, recent studies tend to show that molecular homoplasies would be in fact prevalent since driven by natural selection. By compiling the homoplastic amino acid substitutions in eukaryotic proteins, Rokas and Carroll showed they were twice as frequent than expected under neutral models of protein evolution (Rokas and Carroll, 2008). At this point, it becomes obvious that no set of traits is able to include or exclude an organism in or from a species since species themselves have great similarities but

heterogeneous members. The essentialist definition of “species” should therefore be definitively rejected.

If a set of traits can not define a species by itself, the frequencies and the persistence of each trait over generations could. After Darwin introduced how species are changing over time (Darwin, 1859b), most of the scientists agreed that an organism belongs to a species because it is part of a lineage and not because it has a particular qualitative feature. Such a lineage could be compared to a continuous entity with a distribution of gene frequency over time and over all the members of the lineage. Considering a trait, a species would thus be

“located” around the maximum of this distribution. This implies that two closely related species will share a common boundary in term of gene frequencies regarding one trait. In the same way, a species under speciation process will change progressively from unimodal to multimodal distribution of gene frequencies. A similar approach of the species concept is given in the “Population Structure Theory” (PST) (Ereshefsky and Matthen, 2005). A species is there defined only by the similarities (or variations) of its members, i.e. its traits distributions. This assumption seems correct and more universal than the essentialist definition which failed to catch the species heterogeneity over time and between specimens.

Nevertheless it weakly defines the concept and rather only describes some of its intrinsic properties. A species is indeed constituted of organisms having, at a given time, a precise distribution of traits frequencies, but does it state on what is a species? In other words, the PST presents a species as a set of individuals having a certain distribution properties regarding a given trait. Thus, the common feature shared by all species and defining them as

“species” should be “to have members non-randomly distributed regarding certain traits”. Yet, this feature is also shared with other entities than species, notably with other taxonomic levels. Therefore, the PST fails to offer any univocal definition of the species category or efficient method to separate closely related species.

A third definition for “species” is given by Ernst Mayr: "groups of actually or potentially interbreeding natural populations, which are reproductively isolated from other such groups" (Mayr, 1942). At first sight, this definition seems to offer a clear distinction between species and appears to be proper to this taxonomic level. Unfortunately, it also raises more questions than it gives answers. First of all, reproductive compatibility criterion does not take into account horizontal gene transfers, which also contribute to species diversification

and distinctness. There are increasing evidences that horizontal gene transfer occurs not only within bacteria and unicellular eukaryotes (Andersson, 2009) but also within plants (Woloszynska et al., 2004), mollusks (Rumpho et al., 2008) and crustaceans (Williamson, 2003). Many biologists assume that two populations with sufficiently different traits (acquired for instance during horizontal gene transfer) should be considered as two distinct species even if they still can interbreed. This remark is especially relevant in microbiology where the interspecies boundary is hazy and horizontal gene transfer common. To resolve such conflict some kind of arbitrary limits have been established depending on the taxonomic groups. For instance, populations of bacteria or archaea having more than 1.3 % differences in the 16S ribosomal RNA gene, are currently considered as distinct species (Stackebrandt and Ebers, 2006). The second objection to the Ernst Mayr’s definition comes from the fact that the interbreeding criterion is actually also a trait, having (like any other trait) a frequency distribution across the members of one single population. This implies that the ability of a specimen to interbreed with another specimen from another population will depend on its

“position” in this distribution. This is illustrated in Fig. 1.1.1. Considering three populations A, B and C closely related and composed of respective subpopulations: A1, A2, A3; B1, B2, B3; C1, a value could be attributed to each subpopulation according to a morphological trait.

For instance, populations of birds could be plotted according to their beak size. Specimen of population A present beaks of different size among subpopulations A1, A2 and A3, with a maximum of individuals in A1, i.e. having a beak of 3 cm length. The situation of population B is similar with three subpopulations B1, B2 and B3 presenting increasing beak sizes with a maximum of individuals in B2, i.e. having a beak of 5 cm length. Considering that the beak size is as a decisive criterion to choose mating partner. If birds of A1, A2 and A3 can potentially interbreed, as well as birds of B1, B2 and B3 without being able to interbreed between A and B, both populations should be considered as distinct species S1 and S2. If birds of C1 can interbreed with A3 and B1, those three populations should also, according to the definition, consist in a species S3. Yet it is impossible, according to the same definition, since S3 is not “reproductively isolated” from S1 and S2. This fictive example show how unclear is the interbreeding criterion in the Ernst Mayr’s definition. If it should be applied to all members of the same species, the definition becomes impractical. But if only few specimen of a population should be able to interbreed for that population to be a species, any population wide enough to include interbreeding members should be considered as species.

Once again, the species concept seems to escape from its own definition.

Figure 1.1.1. Distribution of a morphological trait as a criterion for species distinction. A1, A2, A2, C1, B1, B2 and B3 represent birds populations and are plotted as a function of their beak size. S1, S2 and S3 represent hypothetical species according to Ernst Mayr’s definition (groups of potentially interbreeding natural populations). Barriers between S1, S2 and S3 can not be established. According to the definition, should A3 and B1 belong to the same species? In one hand, they are reproductively isolated but on the other hand, they are regrouped by C1, which can interbreed with both A3 and B1.

To conclude, it should be assumed that there is no universal definition of “species”

simply because this category does not exist in the nature. Indeed, species vary in the way they regroup organisms, do not have a common definition but rather common characteristics like a non-random distribution in the traits frequency of their members. Darwin also wrote:

“I look at the term species as one arbitrarily given for the sake of convenience to a set of individuals closely resembling each other (...) It does not essentially differ from the word variety, which is given to less distinct and more fluctuating forms. The term variety, again, in comparison with mere individual differences, is also applied arbitrarily, and for convenience sake." (Darwin, 1859a).

Eventhough the existence of species category (i.e. taxonomic level) has to be rejected;

there should be no doubt about the use of the species taxa (like for instance Raphus cucullatus or Epistominella exigua) as the first and foremost convenient evolutionary units, which representatives have been arbitrarily chosen and which traits evolve over space throughout their representatives and over time from their appearance to their extinction.

Species distinction according to a morphological trait