What is a species? Even Darwin got it wrong.

What is a species? Even Darwin got it wrong.

Tim Crowe, Tshifhiwa Mandiwana-Neudani, Potiphar Kaliba and Muthama Muasya

3907 Conservation reads

Depending on your concept of species, there was – and still is - only one

or as many as 17 species of humans (Homo).

http://www.jstor.org/stable/10.1086/377663?seq=1#page_scan_tab_contents  

How do non-literate folk name ‘species’?  Do they use biological criteria that reflect anatomical, behavioural and ecological similarities/differences? Or, do they partition life from a functional perspective, emphasizing utilitarian, materialistic, cultural, symbolic or spiritual criteria? http://science.sciencemag.org/content/204/4391/381 Are biological species ontologically ‘real’ entities or artificial constructs created (as depicted above) by ‘dry’ old taxonomists https://www.vocabulary.com/dictionary/taxonomist  studying dead things in natural history museums and herbaria? http://www.blackwellpublishing.com/ridley/tutorials/The_idea_of_a_species22.asp  How do modern comparative biologists view species as evolutionarily significant products?  http://onlinelibrary.wiley.com/doi/10.1111/j.1463-6409.2008.00381.x/abstract;jsessionid=1C27F126BB3E62FD195282EFB5E5FDAC.f04t04?userIsAuthenticated=false&deniedAccessCustomisedMessage=   Is there a universal species concept that can be employed by lay people and scientists to classify all life forms?  http://bioscience.oxfordjournals.org/content/early/2016/03/21/biosci.biw026.full

Some background - We are systematists who study the theory/practice of discovering/describing/naming species (taxonomy) and their evolutionary tree-like relationships (phylogenetics).  TC, although born and raised in the USA, has studied the systematics of a broad range of African birds (and odd invertebrates) for 40+ years.  T M-N comes from rural Venda, South Africa, and studies ‘francolins’, a diverse group of African gamebirds.  PK comes from Malawi and has studied birds and mammals within the Malawi Rift region leading to systematic conservation planning/management.  MM grew up among the Akamba, a bantu group from eastern Kenya, and has studied the systematics a broad range of plants in the Savanna and Fynbos Biomes. 

Folk taxonomy – The leading authority in ethno-taxonomy is Brent Berlin.  He and his collaborators have demonstrated humans’ cross-cultural “largely unconscious appreciation of the natural affinities among groupings of plants and animals … quite independently of [their] actual or potential usefulness or symbolic significance in human society".   https://www.google.co.za/?gfe_rd=cr&ei=v6zBV7LTN4up8weTwo6IBQ#q=Berlin%2C+B.+(1992).+Ethnobiological+Classification:+Principles+of+Categorization+of+Plants+and+Animals+in+Traditional+Societies

Our African experience with plants and animals supports Berlin’s view, but folk species are often not partitioned finely.   For example, the Akamba group species relatively broadly: nzoka - snakes; nyunyi - birds; nyeki – grass-like plants.  Only charismatic and/or useful taxa have the equivalent of biological species names.  In Malawi, bird names used by the three major ethnic groups (Tumbuka, Chewa and Lhonwe) tend to recognize the same ‘species’ and partition them somewhat more finely than the Akamba, but still only down to the equivalent of biological genera.  The seminal ethno-taxonomic studies for South African trees and birds are by Louis Louwrens and suggest the same is true for Northern Sesotho speakers.  http://africanlanguages.com/sdp/ff/  The correspondence between bird and scientific names for birds is much better for isiZulu speakers (Chadwick – Ostrich – 1947: 179-182).

The bottom line is that, although African folk ‘taxonomy’ does not neatly reflect biological taxa, humans appear to have an “innate” interest/ability in naming biologically meaningful entities.  Taxonomy may thus vie for the title “oldest profession”.

Are biological species ‘real’? –   It depends on what constitutes ‘reality’.  We maintain that anatomically/ecologically/behaviourally distinct, sexually-reproductively-isolated species are real spatio-temporally bound, evolutionarily-separated ‘individuals’. 

https://books.google.co.za/books?id=jPAjv5FsKMYC&pg=PA231&dq=species+as+individuals&hl=en&sa=X&ved=0ahUKEwiH9JmTlMXNAhXGIcAKHcfaA24Q6AEIHDAA#v=onepage&q=species%20as%20individuals&f=false  But, there are problems.   

First, like all ‘individuals’, species ‘die’ when their last population goes extinct.  However, since species are comprised of multiple populations, they do not arise from a single ‘birthing’ event.  What actually happens is that, due to natural selection and random genetic drift http://projects.nfstc.org/pdi/Subject07/pdi_s07_m01_02_d.htm, multiple populational lineages (branches of evolutionary trees) coalesce from genetically ‘chain-link fence-like’ relationships over evolutionary time into an effectively single lineage.  Populations occupying this branch are characterized by sets of diagnostic attributes (characters), and may even become reproductively isolated from those forming other lineages.  Until that happens, interbreeding between incipient species can undermine their ‘birth’.  Depending on the study material available, e.g. fossils or complete specimens collected in nature and species concept applied, the number of species recognized can vary enormously.  For example, one to as many as 17 species are attributed to the genus Homo.  http://www.jstor.org/stable/10.1086/377663?seq=1#page_scan_tab_contents  Then, of course, there are asexually reproducing ‘species’.  We will deal with them later.

Regardless, species are ‘real’ entities out there to be discovered, named, studied and conserved.

Discovering/delineating species

Typological Concept - In pre-evolutionary taxonomy, Carolus Linnaeus (1707–1778) used of gross anatomical similarity to identify ‘typologically’ distinct species.   http://www.famousscientists.org/carolus-linnaeus/  But, well before Darwin’s time, some taxonomists expressed concern that typologically distinct ‘species’ that interbreed may warrant only the rank of subspecies (= race).  Field-oriented biologists were also concerned that anatomically similar populations that differ distinguishably ecologically and behaviourally form valid ‘cryptic species’.   In his On the Origin of Species, Darwin took no or, at best, an authoritarian position http://darwin-online.org.uk/converted/pdf/1861_OriginNY_F382.pdf :

“there is no infallible criterion by which to distinguish species and well-marked varieties”

“the opinion of naturalists having sound judgement and wide experiences

seems the only guide to follow”.

Biological (Isolation) Concept - During much of the 20^th Century, many vertebrate zoologists adopted the reproduction-based Biological Species Concept (BSC).  BSC species, irrespective of anatomical distinctiveness, are “protected gene pools” separated from one another by intrinsic pre-mating (e.g. male/female displays) and/or post-mating (e.g. embryonic death/offspring sterility) reproductive isolating “mechanisms”. http://www.evolution.berkeley.edu/evosite/evo101/VA1BioSpeciesConcept.shtml 

The major challenges to the BSC are allopatric (geographically isolated) anatomically distinct populations (incipient species) which don’t have the opportunity to interbreed, and low-moderate hybridization between parapatric (allopatric, but geographically ‘touching’) ones.  In the former case, taxonomists focus on character differences that may influence mate recognition (e.g. calls in birds and amphibians).  In the latter, the entities are considered as separate species if there is assortative mating within incipient species when they come into contact or hybrids have lower fitness (in the worst case – sterility). 

Recognition Concept - During the 1970-80s, Hugh Paterson turned the BSC on its head, maintaining that it was specific-mate recognition systems (genetically ‘hard-wired’ anatomical compatibility of genitalia, sperm and eggs, mating behaviours/calls, pheromones, etc.) that unite species’ populations, rather than isolating mechanisms that separate them. https://books.google.co.za/books?id=D1PwAAAAMAAJ&q=specific-mate+recognition+systems+paterson&dq=specific-mate+recognition+systems+paterson&hl=en&sa=X&ved=0ahUKEwji9uPRkcXNAhUFBMAKHbXVA1AQ6AEIKjAA  Thus, if males and females attempt to interbreed and fertilization occurs, they belong to the same species.

Phenetic Concept - Taking an extremely alternative, arguably anti-evolutionary view, other taxonomists argued that species can be discovered/delineated using assessment of average, overall similarity in anatomical form (morphology http://www.oxforddictionaries.com/definition/english/morphology).  This involves using multi-variate statistical procedures based on many, equally weighted (i.e. not favouring those involved with reproduction or other ‘important’ biological processes) attributes expressed as quantitative measurements.  Species, in this case, are populations that differ overall by some ‘empirically determined’, average level of morphological difference.  This approach was labelled ‘phenetics’.  http://www.annualreviews.org/doi/pdf/10.1146/annurev.es.17.110186.002231  Francis Thackeray has recently used a phenetic species concept to investigate the   species status of Homo neledi.   http://sajs.co.za/sites/default/files/publications/pdf/SAJS%20111_11-12_Thackeray_Sci%20Cor.pdf

Some molecular pheneticists insist that species may be also delineated using an ‘empirically determined’ level of overall divergence in DNA.  The best example of this is DNA ‘barcoding’ which maintained that vertebrate species are entities that differ by >2% in the mitochondrial gene, cytochrome c oxidase I (COI).  http://www.ncbi.nlm.nih.gov/pmc/articles/PMC518999/

Ecological Concept - Some ecologists dissatisfied with reproduction/morphology-based species concepts favour ecological species – anatomically distinct (but interbreeding) groups of populations commonly adapted anatomically and physiologically to a particular set of resources and selective pressures (diet, fire and water uptake), called a niche or adaptive zone. http://www.blackwellpublishing.com/ridley/a-z/Ecological_species_concept.asp  They are less concerned with interbreeding and more interested in recognizing adaptive ‘solutions’ to environmental challenges.

Evolutionary/Phylogenetic Concepts - Finally, taxonomists intent on discovering distinct evolutionary lineages have promoted the ‘evolutionary’ and ‘phylogenetic’ species concepts.  http://sysbio.oxfordjournals.org/content/27/1/17  The former is somewhat nebulously defined – “a lineage of ancestral descendant populations which maintains its identity from other such lineages and which has its own evolutionary tendencies and historical fate.”  The latter involves identifying a lineage whose members are descended from a common ancestor and who possess a unique combination of evolutionarily novel and ancestral characters. http://www.encyclopedia.com/topic/phylogenetic_species_concept.aspx

How many species exist?

Depending on your species concept, different numbers of species are recognized.  By setting the outer limits of sexual species to mate recognition, Paterson’s concept accepts the fewest.  The BSC recognizes more species, but relies heavily on the use of races/subspecies to ‘downgrade’ geographically diagnosable, occasionally hybridizing groups populations.  During the first two-thirds of the 20^th Century, this practice resulted in a huge drop in the number of species (for birds from about 19 000 in the early 1900s to around 8 600 in 1980) and a massive increase in trivial, taxonomically questionable races/subspecies. http://www.amerika.org/nature/subspecies-and-classification/  This disparity created an enormous problem for conservationists who need biodiversity inventories to prioritize taxa and areas for conservation action. 

The ecological species concept has not been applied broadly, but would probably recognize more species than the BSC, but fewer if subspecies come into play. 

If taken to the extreme, with the availability DNA evidence  http://www.pitt.edu/~jhs/articles/molecular_systematics.pdf and sophisticated phenetic/morphometric techniques developed since the 1980s https://www.researchgate.net/publication/247548080_Book_Review_Morphometrics_in_Evolutionary_Biology_The_Geometry_of_Size_and_Shape_Change_with_Examples_from_Fishes_Special_Publication_15_Fred_L_Bookstein_Barry_Chernoff_Ruth_L_Elder_Julian_M_Humphries, it is now possible to delineate an astronomical number of  ‘species’.  Some misguided/‘toxic-taxonomists’ have even used these ‘forensic’ techniques to distinguish five or more different ‘races’ amongst Homo sapiens.  http://theconversation.com/how-science-has-been-abused-through-the-ages-to-promote-racism-50629   Palaeontologists working with fragmentary bits-and-pieces fossils frequently ‘over-split’ them into species to emphasize morphological differences: hence the proliferation of ‘species’ of Homo.

What to do? -   We prefer a novel concept, the Consilience Species Concept (CSC), that incorporates useful features of those outlined above.  A CSC species as distinct evolutionary lineage comprising populations that are diagnosable using a suite of heritable, complementary, arguably independent characteristics (qualitative anatomical, behavioural, ecological, physiological and molecular genetic) that show consilient, multifaceted variation.  http://dx.doi.org/10.1111/j.1474-919X.1994.tb01081.x  The term consilience (a "jumping together" of knowledge) was coined by philosopher William Whewell. http://plato.stanford.edu/entries/whewell/   In simple terms: “If it walks like a duck, quacks like a duck, water ‘rolls’ off its back, has webbed feet and a flattened bill, it’s a duck”. 

Thus, academic and ‘citizen’ scientists http://www.birds.cornell.edu/citscitoolkit/about/definition should consider evidence from a range of independent sources and delineate species on the basis of consilient, concordant evidence and not on ability to interbreed (or not) or some arbitrary amount of overall difference in anatomy or DNA composition.  The CSC is superior to its competitors because, by design, it prevents the recognition of huge numbers of trivial taxa and does not ignore evolutionarily significant entities because they interbreed.  Furthermore, it can be applied consistently to both sexual and asexually reproducing ‘species’.