‘For the survival of the species’: The mismatch between evolutionary biology and conservation biology...and 'taxonomic inflation'

'Jock' Marshall
from here

In the 1960s there was a board for newspaper clippings, notices and other ephemera on the corridor wall of the old zoology floor in the now-demolished Northcote Science Building at the University of Hong Kong. At the top was a cutting from an Australian newspaper reporting an interview with the larger-than-life Professor Alan John ‘Jock’ Marshall (1911-1967) then at Monash University in Melbourne. The clearly shocked journalist reported words to the effect that Marshall did not care what happened to individual animals; what did concern him was conserving species and if that meant some individuals dying in the process then so be it.

That, in a nutshell, describes the fundamental mismatch between evolutionary biologist’s view of species compared with that of the early conservation movement and hence, because of the publicity given to conservation activities, that of the public. So we have, on the one hand, biologists wincing when they hear ‘for the survival of the species’ in terms of natural selection while at the same time conservationists talk of their work ‘for the survival of the species’.

Early conservation efforts were seen as direct threats to large animals and in terms of getting the public and politicians engaged with he problem there is nothing so persuasive as a member of the charismatic megafauna. The World Wildlife Fund’s choice the Giant Panda is the most famous example. While there were—and still are—direct and major threats to the survival of individual species, the poaching of rhinoceroses being a prime example, the question of preserving habitats (or whole ecosystems, although I hate the term because it is misleading) tended to be put to one side. If you can conserve the large species, then there will be sufficient habitat for the smaller ones to be protected as well.

However, when it came to national conservation politics legal protection was often based on a species and not on a habitat. Across a wide geographical area, local extinctions from habitat loss or hunting were possible because the species there were either not sufficiently endangered or represented a very small proportion of the total population of the species. So, the pressure was on to increase the number of species by elevating geographical variants (often termed, probably unwisely, as subspecies) to the status of full species. But not only do conservation efforts benefit (if only at first sight) by increasing the number of species. Birders of the tick-list variety just thrive on species being ‘split’ and the tour companies are always at pains to point out the chances of seeing a a new ‘split’ in a particular area. The tourism industry also loves a distinctive name for their familiar animal. ‘This is Thornicroft’s giraffe, madam’ said the guide in Zambia who was surprised when madam replied, ‘Just a giraffe with a geographically distinctive pattern’.

The whole process of increasing the number of species by deviating from the biological species concept has been called ‘taxonomic inflation’. The increase is not new; some taxonomists of old split species ad nauseam but after dismissing the nonsensical claims there were reckoned to be 4,659 mammals in 1993. By 2005 that number had risen to 5,418, not as explained by Shai Meiri and Georgina Mace in their 2007 paper, by an increase in the discovery of new species but by the splitting of existing species. With mammals, that splitting has occurred to the greatest extent in Africa where a species may have a widespread distribution.

Meiri & Mace continued:

Most of these recently described species are allopatric or parapatric (i.e., with ranges that abut but do not overlap) populations, separated by barriers such as rivers. Given a barrier to gene flow, the accumulation of genetic and morphological differences is expected and may be of limited biological importance. It seems, however, that many recent taxonomic studies regard the presence of allopatric populations as an indication that speciation has occurred. We suggest that stronger evidence is needed to show that populations are sufficiently distinct to merit specific status. This evidence should be capable of discriminating genuine ecological and evolutionary distinctiveness from minor differences that could result from geographic isolation.

I am not going into the various species concepts here but the taxonomists who do such splitting rely on using genetic analyses to identify different lineages. Some—the ‘splitters’—then argue that if groups of animals show distinct genetic lineage then they should be treated as different species, regardless of the fact that morphological differences are minor or that members of one lineage recognised those of anther as being of the same kind and would breed with them if given the chance and do do so in captivity.

While ‘new’ species may at first sight be an attractive proposition for those seeking the input of conservation resources, Meiri & Mace argued that with limited funding, resources could be diverted from a really important projects and that splitting species does not necessarily have conservation value. They also supported the policy of supporting species ‘across their ranges, perhaps favoring phenotypically distinct populations or geographically isolated subsets so as to fully conserve variation’.

Have those lessons so well spelt out by Meiri and Mace been learnt? Was madam right about Thorncroft’s giraffe?

Meiri S, Mace GM. 2007. New taxonomy and the origin of species. PLoS Biol 5(7): e194. doi:10.1371/journal.pbio.0050194

Genomes show why Hooded and Carrion Crows are different and stay different…and are they different species?

Over the years, as an outsider to the field, I have read about taxonomy and systematics and I have read about different species concepts and the attempts to define what species are. It has struck me that the whole discussion has been concerned with defining the species as a group as opposed to considering the individuals that make up that group. I just have the feeling that defining the group without reference to the individual came from an age when many if not most biologists argued intentionally or unintentionally for group selection with, for example, adaptations ‘important for the survival of the species’ on many lips. As the realisation grew that group selection was the result of flawed reasoning and that the individual is the unit of selection, nobody to me, or at least nobody that I could find, was writing about the species as a collection of individuals subject to natural selection (although this view does seem implicit in the Grants’ work on Galapagos finches). When I did consider the individual I realised that for many organisms, most vertebrates, for example, a species could be defined as those individuals with which an individual could breed to its selective advantage or to put it the other way round, with which an individual could breed without selective disadvantage. Therefore, to me the group—the species— is defined by the advantage it affords its individual members in terms of fitness.

My amateur definition includes those species identified as being completely reproductively isolated (i.e. those that conform to the Biological Species Concept as originally propounded) as well as those, like the Galapagos finches, in which there is gene flow between obviously different species or in which there is a hybrid zone between geographically adjacent forms that differ morphologically and/or behaviourally.  I therefore bridle when I hear only the former referred to as ‘good’ species by those wedded to the Biological Species Concept, with the others left to a ‘judgement call’ as to their status; ‘easily discernible’ should replace ‘good’.

To reiterate, my definition means that complete reproductive isolation (i.e. no gene flow) is not necessary in order to define a species. This definition provides for breeding between neighbouring closely related forms with a hybrid zone between them. If breeding with the other neighbouring form leads to the hybrid offspring having a selective disadvantage then the two forms are retained as distinct species even though introgression occurs.

It is with background that I read a recent paper in Science with great interest. Not only does it throw light on the species problem, it also occurs on my doorstep. The paper, The genomic landscape underlying phenotypic integrity in the face of gene flow in crows, is on the genetic differences between the Hooded Crow and Carrion Crow. It is also interesting not only in its own right but also for the comments it evoked from those trying to decide whether the two crows should be regarded as one or two species.

We live fairly near the hybrid zone between the Hooded and Carrion crows in the West of Scotland. A hybrid lived for several years in the surrounding gardens and school playing field even though it never looked the healthiest of birds and had, what the vets would described as, an ‘unthrifty’ appearance. As well as hybrids, Hooded Crows are reported occasionally since the hybrid zone is narrow at this point and hoodies occur on the islands of Arran and Ailsa Craig where they are said to prefer the higher ground compared with the Carrion Crow.

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Carrion Crow

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Hooded Crow


Discussion has centred on whether the new findings offer support to the arguments in favour of considering the two forms as two species, or as subspecies of one species. Over the years they have flitted between being regarded as two species or one. Linnaeus originally described them as two species but throughout the later part of the 20th century, the one species view prevailed with the Hooded Crow listed as a subspecies, Corvus corone cornix, alongside the Carrion Crow, C. c. corone. Then, in 2002 the British Ornithologists’ Union recommended that the two forms should be recognised as separate species (Knox et al 2002). The reasons for this (non-random mating and reduced fitness of the hybrids) and how they fit the Evolutionary Species Concept are explained by Parkin et al  (2003) and by Parkin (2003). Parkin (2003) concludes:

In the case of the crows, I believe that the Hooded and Carrion lineages maintain their separate identities through time and space, for hybrids are at a selective disadvantage. They should be regarded as separate species.

The work that has caused the flurry of interest was done on mainland Europe by Swedish, German and Spanish co-authors (Poelstra et al 2014). They compared Carrion Crows from Spain and Germany with Hooded Crows from Poland and Sweden (as in northern Britain there is a hybrid zone where the two forms meet). The differences detected in the genome and in gene expression have been described and discussed well elsewhere, for example, in a commentary in Science by Peter de Knijff. I will only state here some of the main conclusions.

Differences between the two forms were very small. Only 83 out of 8.4 million DNA positions were found to be fixed and therefore diagnostic of the two forms. As one would expect, the genes concerned were mainly associated with plumage colour. Of the 83 fixed differences 81 were found in a small region of chromosome 18.

de Knijff summed up the conclusions neatly: Poelstra et al. present a unique case of speciation whereby, despite substantial gene flow (especially from hooded crows into German carrion crows), phenotypic divergence likely caused by assortative mating and sexual selection is maintained by genetic variation in less than 1% of the genome. Invoking Darwin on species concepts he concludes: Obviously, forcing complex patterns of biological variation into a single hierarchically structured archive is a purely anthropogenic project. No matter how hard we try, there cannot be a robust, all-inclusive, objective species concept.

While the latter sentence is probably right, I am not sure that the concept of a species is entirely anthropogenic. Defined from the fitness of individuals, an assemblage does have some sort of real existence at an ecological level for example. What I am now convinced is that the Biological Species Concept has had its day in its classical mid-20th century form. It is and perhaps always was too dogmatic; its underlying hypothesis is simplistic and has been undermined by further observations and experiments. Evolution is more complex than that…and continues.

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de Knijff P. 2014. Carrion and hooded crows defeat Linnaeus’s curse. Science 344 1345

Knox AG, Collinson M, Helbig AJ, Parkin DT, Sangster G. 2002. Taxonomic recommendations for British birds. Ibis 144 707–710

Poelstra JW, Vijay N, Bossu CM, Lantz H, Ryll B, Müller I, Baglione V, Unneberg V, Wikelski M, Grabherr MG, Wolf JBW. 2014. The genomic landscape underlying phenotypic integrity in the face of gene flow in crows. Science (20 June 2014) 344 1410-1414

Parkin DT, Collinson M, Helbig AJ, Knox AG, Sangster G. 2003. The taxonomic status of carrion and hooded crows. British Birds 96 274–290

Parkin DT. 2003. Birding and DNA: species for the new millennium. Bird Study 50 223-242