What is a species?
Philosophers think a lot. Sometimes they think so much that they get entangled in their own thoughts and do not see the flaws in their reasoning (theology is the perfect example of this). Henry Taylor – a philosopher from the University of Birmingham – wrote an article on The Conservation in which he claims that species do not exist. He argues that we should scrap the idea of a species and “think of life as one immense interconnected web.” His article has already been criticized by evolutionary biologist Jerry Coyne. I recently published a book chapter on avian species concept, so this is a nice opportunity to summarize this chapter and correct the sloppy reasoning of this philosopher.
We know what a species is…in theory
After a general introduction about taxonomy, Taylor writes the following sentence: “So, what even is a species? The truth is, we don’t really have any idea.” Actually, we do have an idea. But to understand the solution to this species problem, we need to make a distinction between the theoretical question of what species are (i.e. species concepts) and the ways in which species can be delimited in practice (i.e. species criteria). From a theoretical point of view, we know what species are. This part of the species problem was independently solved by Richard Mayden and Kevin De Quieroz.
Richard Mayden examined 22 distinct species concepts and proposed a hierarchy of species concepts, with a primary theoretical species concept and several secondary operational species concepts. He argued that only one concept is suitable as primary concept, namely the Evolutionary Species Concept: “A species is an entity composed of organisms which maintains its identity from other such entities through time and over space, and which has its own independent evolutionary fate and historical tendencies”. The remaining, secondary concepts function as guidelines that are essential for the study of species in practice. So, they are actually species criteria instead of concepts.
Similarly, Kevin De Queiroz reviewed several existing species concepts and argued that all existing species concepts are variants of a single general concept, which he dubbed the General Lineage Concept. Species are considered separately evolving metapopulation lineages. A lineage indicates an ancestor-descendant series, and metapopulation refers to an inclusive population made up of connected subpopulations.
The hierarchy of species concepts with an overarching primary concept (i.e. the Evolutionary Species Concept) and several secondary concepts that are used as criteria. From: Mayden (1997) Species: The units of diversity.
A Life History Approach
So far, so good. From a theoretical point of view, we can define species according to the Evolutionary Species Concept and the General Lineage Concept. But what about species delimitation in practice? Which secondary concepts should we use? That choice will depend on the evolutionary history of the species in question. Here, a “life history approach” is warranted, in which different species concepts correspond to different stages in the life history (i.e. speciation process) of a species.
It is important to keep in mind that the order in which species concepts arise is contingent upon the speciation process. In some cases, morphological differentiation might evolve first, followed by reproductive isolation. In other cases, it might be the other way around. And in yet other cases, some species concepts will not apply.
Moreover, during the speciation process, there will be a grey zone in which different species criteria come into conflict. For example, several putative species of Redpoll Finches (genus Acanthis) are morphologically different despite largely undifferentiated genomes. There is a conflict between a morphological and a genetic species concept. What should taxonomists do now? The answer is integrative taxonomy.
This simplified diagram represents a single lineage splitting into two independently evolving lineages (or species). The horizontal lines represent the times at which the lineages acquire different properties (e.g. they become phenetically distinguishable, reproductively isolated, reciprocally monophyletic, etc.). This set of properties (SC species concept) coincides with a grey zone in which alternative species concepts come into conflict. On either side of the grey zone, there is agreement on the number of species. Adapted from De Queiroz (2007) Systematic Biology.
The rationale behind integrative taxonomy is quite straightforward: different taxonomic concepts and methods are integrated in the delimitation and description of species. A recent paper on taxonomic bird studies found that nearly half (46.5%) applied multiple criteria in species delimitation. Within this context, two general frameworks have been advocated: integration by congruence and integration by cumulation.
The congruence approach to species delimitation entails that different data sets, such as molecular and morphological characters, support the decision to recognize certain taxa as valid and distinct species. For example, Per Alström and his colleagues used congruence between plumage, biometrics, egg coloration, song, mitochondrial DNA and distribution to draw species limits in the Bradypterus thoracicus complex. The main advantage of this approach is that most taxonomists will agree on the validity of a species supported by several independent data sets, leading to taxonomic stability.
The alternative framework, integration by cumulation, is based on the assumption that any of the data sets can be used as evidence for the delimitation of species. Congruence is desired but not necessary. In practice, evidence from different data sets is cumulated, concordances and conflicts are explained within the specific evolutionary context of the taxa under study, and based on the available evidence a decision is made. An advantage of this approach is that species delimitation is not restricted by one particular biological property.
Species limits in the Bradypterus thoracicus complex were determined using an integrative approach based on several criteria. From: http://www.hbw.com/
An Interconnected Web
I hope that the explanations above have convinced you that species do exist and that we can define them in practice (although drawing species limits is not always straightforward). What about the statement by Henry Taylor that “we should think of life as one immense interconnected web.” I agree with this statement but it does not lead to the conclusion that species do not exist.
Hybridization is a common phenomenon (as this website clearly shows for birds). Numerous species are known to exchange genetic material through hybridization. But does that invalidate their rank as distinct species? No, despite the occasional genetic contribution of other taxa, species tend to maintain their own identity with their own independent evolutionary fate and historical tendencies (as stated by the Evolutionary Species Concept).
In the end, Taylor writes that “there is no such thing as ‘the human species’ at all.” He does not explain the exact reasoning behind this bold statement, but I assume he refers to the interbreeding between humans, Neanderthals and Denisovans. Does gene flow between these members of the genus Homo result in the disappearance of the species Homo sapiens? Of course not! The genes that we obtained from Neanderthals and Denisovans have certainly influenced our consequent evolution but overall the human species has maintained its own identity with its own independent evolutionary fate and historical tendencies (sorry to repeat this concept, but I really want to drive the point home here).
The complex evolutionary history of humans with multiple events of interbreeding with Neanderthals and Denisovans. From: Callaway (2016) Nature
Avian Species Concepts in the Light of Genomics
I will end my discussion of the species problem here. To summarize, the species problem can be partly resolved by theoretical monism (the evolutionary species concept or general lineage concept) in combination with practical pluralism, in which different species criteria correspond to different stages during the speciation process.
In my book chapter on species concept, I focused on the role of genomics in this debate. If you are interested in this question, feel free to contact me for a PDF of the chapter. I will paste the main points from the abstract below:
In this chapter, I argue that genomics provides another line of evidence in this pluralistic approach to species classification. Indeed, genomic data can be combined with classical species criteria, such as diagnosability, phylogeny and reproductive isolation. First, genomic data can provide an extra diagnostic feature in species delimitation. Compared to ‘old-school’ genetic markers, the use of genome-wide markers leads to a significant rise in statistical power. Second, phylogenomic analyses can resolve the evolutionary relationships within rapidly diverging or hybridizing groups of species while taking into account gene tree discordance. Third, genomic data can be used to pinpoint the genetic basis of reproductive isolation and provide a detailed description of the speciation process. All in all, the genomic era will supply avian taxonomists with a new tool box that can be applied to old concepts, leading to better informed decisions in cataloguing biodiversity.
Ottenburghs, J. (2019). Avian species concepts in the light of genomics. In Avian Genomics in Ecology and Evolution (pp. 211-235). Springer, Cham.