The application of species concepts to marine organisms: do we need a
new species concept?
It is commonly accepted within the scientific community that ‘species’ is a fundamental natural unit
(Ridley, 1996). However scientists are often unable to agree on exactly what a species is, and how it
should be defined. At first the differences between species seem fairly straightforward, different
species look different, live in different ways and in different environments. These differences seem
sufficient to establish one species from another for most animals and plants. However there are
several cases in nature where these simple differences are not enough to enable biologists to
distinguish one species from another. This essay will look at some of those examples taken from the
marine environment and I will show how biologists have approached the situation using different
species concepts. I will start by illustrating six of the main species concepts in use today and
illustrating their respective advantages and disadvantages.
There are many different proposed species concepts, each of which uses different factors in order to
establish species. These species concepts can be grouped into two main classes, these classes are
non-temporal and temporal. Non-temporal (also called non-dimensional) species concepts aim to
identify the members of a species at a particular time, i.e. without regard to their ancestral past
(Ridley, 1996). Whereas temporal species concepts takes account of the temporal dimension of
evolution and aims to specify which individuals are members of a species not only at one time, but
throughout all time (Ridley, 1996).
Traditionally the most commonly used non-temporal species concept is the phenetic or
morphological species concept, indeed this concept was used by Charles Darwin (Mallet, 1995).
The phenetic species concept defines a species as a set of organisms that look similar to each other
and distinct from other sets (Ridley, 1996). It uses only phenotypic characteristics in order to judge
whether or not an individual is the same species as another individual. In practice the phenetic
concept has numerous limitations one of the main problems arises when confronted with sibling
species. Sibling species are common in all major marine habitats (Knowlton, 1993). Sibling species
are species that are difficult or impossible to distinguish based on morphological characters
(Knowlton, 1993). This exposes major flaws with the phenetic species concept, if two species have
such similar phenotypic characteristics as to make them indistinguishable from one another then the
whole basis of the phenetic species concept becomes irrelevant. The need then arises to use other
techniques and species concepts in order to differentiate between the species. The phenetic species
concept uses measures of as many characters as possible in as many organisms as possible (Ridley,
1996).
Knowlton (1993) illustrates one of the main problems with the phenetic species concept in her
paper ‘Sibling species in the sea’. In the paper she states that sibling species are species that are
difficult or impossible [my italics] to distinguish based on morphological characters (Knowlton,
1993). Indeed the existence of sister species has formed a major part of Mayr’s attack on the
phenetic species concept in favour of the biological species concept (Knowlton, 1993). Some
marine groups exhibit many examples of sibling species, for example sponges with their lack of
recognisable features (Knowlton, 1993). However sibling species are not restricted to ‘lower’ levels
of life. Only in the 1980’s have the species complexes in European periwinkles been clarified, and
there is still controversy regarding the classification of the edible European Mussel (Knowlton,
1993; Gosling, 1994).
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Another common species concept is the Biological or Isolation species concept. It was Ernst Mayr
in 1942 who produced the biological species concept (Majerus, 1996). The concept states that
species are ‘groups’ of actually or potentially interbreeding populations which are reproductively
isolated from other such groups (Mayr, 1942). In other words the biological species concept states
that species are groups of interbreeding natural populations that are reproductively isolated from
other such groups (Ridley, 1996). The biological species concept has been the dominant one in the
evolutionary literature since the 1940s (Gosling, 1994). In theory the isolation species concept
delimits species on the basis of non-interbreeding. However in practice the fact that there is so little
information on the breeding capabilities of the vast majority of species means that often those using
the isolation species concept, ultimately have to resort to morphological characteristics (Gosling,
1994).
The Recognition species concept is closely related to the biological species concept, however
instead of defining species by interbreeding and reproductive isolation the recognition species
concept uses shared mate recognition systems (SMRS). It has been claimed by Paterson (1981) that
the recognition technique of species definition can offer a number of advantages over the biological
species concept. Firstly mate recognition can often be observed in a few, even dead, specimens,
whereas interbreeding is more difficult to observe and is usually inferred indirectly (Ridley, 1996).
The second possible advantage is more theoretical. The recognition species concept may be a more
accurate technique to show what happens when a new species originates. According to Paterson
(1981) the crucial event for the origin of a new species is the evolution of a new mate recognition
system.
According to the Ecological Species Concept populations form the discrete phenetic clusters that
we recognise as species because the ecological and evolutionary process controlling the division of
resources tend to produce those clusters (Ridley, 1996). Research has shown that the differences
between closely related species living in the same area, are often related to differences in the
ecological resources that the species exploit (Ridley, 1996). Therefore the ecological species
concept defines a species as a set of organisms occupying a single, identical niche.
The Cohesion Species concept was introduced by Templeton and it is largely genetic based. The
Cohesion concept groups individual organisms together with other organisms possessing the same
mosaic of genes. The cohesion species concept does have problems however, when trying to
distinguish closely related species the technique can prove unreliable. However genetics can
produce some remarkable results when investigating sibling species in the marine environment
(Knowlton, 1993). It has been shown that many sibling species who look almost identical often
have major genetic differences (Knowlton, 1993). Another use of genetic similarity between
organisms has shown that the morphologically distinct European and American lobsters are in fact
closely related and in a sense could also be defined as sibling species (Knowlton, 1993).
So far all the species concepts which have been discussed have all been non-temporal concepts, i.e.
they explain how a group of individuals should be grouped into species at one instant (Ridley,
1996). However species last for many generations and it is possible to assume that another species
concept may be needed in order to include all members of a species throughout existence (Ridley,
1996). The most highly regarded of these temporal species concepts is the phylogenetic species
concept which was first described by Cracraft in 1983. The phylogenetic species concept identifies
a species as a group of individuals who share a common evolutionary fate through time which is
diagnosable on the basis of one or more genetically determined traits (Gosling, 1994). The concept
can therefore be applied to both sexual and asexual organisms as well as living and extinct
organisms (Gosling, 1994). The versatility of the phylogenetic species concept has made it an
instant success with evolutionary biologists, taxonomists and palaeontologists (Gosling, 1994),
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however one problem with the concept is that it is often difficult deciding which traits are the
important ones to use in defining a species (Gosling, 1994).
Gosling’s 1994 paper ‘Speciation and wide-scale genetic differentiation’ used three different
‘species situations’ in the marine environment to illustrate the operational usefulness of the species
concepts discussed above. First Gosling compared two cockle species, Cerastoderma edule
(Common cockle) and Cerastoderma glaucum (Lagoon cockle). The two species are almost
identical and the two are frequently confused (Gosling, 1994; Hayward et al, 1996) and it is
believed that the ancestor of the modern species existed about 50 mya (Gosling, 1994). Gosling
(1994) showed that both species are reproductively isolated from each other, therefore good species
using both the isolation and recognition species concepts. The species also displayed sufficient
genetic difference to satisfy the cohesion species concept (Gosling, 1994). And although Gosling
found no evidence that each species constitutes a separate lineage, i.e. is monophyletic, the degree
of differentiation between the two taxa indicated that they were diagnosably distinct, therefore
satisfying the other main requirement of the phylogenetic species concept (Gosling, 1994).
The second group of organisms studied by Gosling were from the order Mytiloida. These were
Mytilus edulis (Common mussel), Mytilus galloprovincialis and Mytilus trossulus. Morphological
differences between the three taxa are small with no single character being clearly diagnostic. The
separate taxa were first identified using allozyme markers (Gosling, 1994). The genus is of
relatively recent origin with apparently no records older than 2 million years (Gosling, 1994). DNA
studies between the taxa have revealed little or no differences (Gosling, 1994). Due to the high
occurrence of hybrids both the isolation and biological concepts become useless. As does the
recognition concept. By the same means there is little evidence of cohesion and so the cohesion
species concept must be dropped. The absence of, to date, of discrete diagnostic characters, at both
morphological and genetic level also makes the application of the phylogenetic species concept
almost impossible (Gosling, 1994). From these results it can be argued that Mytilus do not merit full
specific status, this creates the problem of what to call the different taxa. It has been suggested that
either, a new ‘semispecies’ status could be applied to them, or species definitions could be loosened
(Gosling, 1994).
The third species complex which was studied by Gosling was the Lasaea genus. The Lasaea genus
consist of minute (<6 mm) hermaphroditic brooding bivalves that inhabit crevices on rocky
intertidal shores (Gosling, 1994; Hayward et al, 1996). It was initially claimed that the genus
consisted of more than 40 species, however more recent studies have pointed towards the view of
the genus being monospecific with Lasaea rubra being the nominal species (Gosling, 1994). The
animals are polyploidy and the genus also exhibits two distinct modes of reproduction and
development. L. australis reproduces by cross-fertilisation and releases it’s young as larvae whereas
all other members of the genus release their young as crawl-away juveniles (Gosling, 1994). Due to
the simple fact that their is no sexual reproduction the isolation and recognition species concepts
can not be applied to the asexual clones produced by the majority of the genus (Gosling, 1994).
Animals in the Lasaea species complex are also too similar to be separated using the phylogenetic
species concept. The final species concept left to consider then is the cohesion concept. Since
clones are sexually isolated and are genetically adapted to their own environmental conditions it is
therefore possible to distinguish between the species using the cohesion concept (Gosling, 1994).
Knowlton et al (1997) carried out an investigation to compare the biological and phylogenetic
species concepts using two cases from the marine environment. The first case study she used was
that of the reef building corals. The coral Montastraea annularis is the most abundant and best
studied coral on Caribbean reefs (Knowlton et al, 1997). The coral exhibits enormous variability in
colony morphology, ranging from massive heads to columns to plates (Knowlton et al, 1997).
These three morphologies have often being treated as separate species and although they do show
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considerable overlap in the date of spawning they do appear to be reproductively isolated by a
combination of barriers to fertilisation or development and differences in the hours of peak
spawning (Knowlton et al, 1997). Using the biological species concept the three morphological
varieties of M.annularis can be classed as distinct species. However with the corals being
genetically similar, if not identical and morphology being very similar within the group, the
phylogenetic species concept can not distinguish between the three ‘morphotypes’ (Knowlton et al,
1997).
The second genus investigated was the Alpheidae. These are commonly known as the snapping
shrimp. The genus are numerous and are difficult to distinguish using conventional morphological
characters (Knowlton et al, 1997). The genus also exhibits fixed allozyme differences and
substantial divergence in mitochondrial DNA (mtDNA) sequences (Knowlton et al, 1997).
Interspecific pairings are not observed in the field and are almost impossible to establish in the
laboratory (Knowlton et al, 1997). In this case the phenetic species concept can not easily
distinguish between the taxa whereas both the biological and phylogenetic concept can.
Research has also been carried out on sea urchins in the genus Echinometra. These animals are
widely distributed in shallow reef environments across the tropical Pacific and Indian oceans
(Palumbi, 1992). There have been found to be four closely related species with slight morphological
differences (Palumbi, 1992). These species show little genetic differences in mtDNA which
suggests recent divergence. The four species exhibit strong reproductive isolation, such as the
failure of sperm and eggs from different species to bind and fuse (Palumbi, 1992). Using the
isolation species concept it is clear to show that these urchins are four separate species. The
phenetic species concept also enables the four species to be differentiated.
By studying the above examples of the application of specific species concepts it seems to me that
the term ‘species’ can never be a finite object. In order for natural selection and evolution to occur,
no species can be completely isolated from its sibling species. I believe that there will always be
overlap between species, ecologically, reproductively and genetically. I do believe however, that the
term ‘species’ deserves its place in modern taxonomy. I believe that one must not try to match all
the criteria required by the many species concepts to every organism. Instead a ‘best-fit’ ideology
must be adopted.
I agree that all species concepts must be taken into account by taxonomists and I also agree with
Mallet (1995) that there is a need for subspecies and ‘varieties of species’ as well as species
categories. I think the best method of defining species is to use what has been termed as the
pluralistic species concept where more than one concept is used to identify a species (Ridley, 1996).
It has been shown that all the main concepts have their limitations. For example the phenetic
species concept can have problems with ‘varieties’ of species, including sexually dimorphic species
as well as polymorphic species (Mallet, 1995). I am inclined to agree with Coyne et al (1988) who
claims that the biological (isolation) concept although it does have it’s problems is still the least
flawed species concept we have, and that the biological species concept is the best way so far
defined.
References
Coyne, J.A., Orr, H.A. & Futuyma, D.J., (1988). Do we need a new species concept?. Syst. Zool.
37(2):190-200.
Gosling, E.M., (1994). Speciation and wide-scale genetic differentiation. In Beaumont, A.R. (Ed.),
(1994).Genetics and Evolution of Aquatic Organisms. Chapman & Hall, London.
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Hayward, P., Nelson-Smith, T., Shields, C., (1996). Seashore of Britain & Northern Europe. Harper
Collins. London.
Knowlton, N., (1993). Sibling Species in the Sea. Annu. Rev. Ecol. Syst. 24:189-216.
Knowlton, N. And Weigt, L.A., (1997). Species of marine invertebrates: a comparison of the
biological and phylogenetic species concepts. In Claridge, M.F., Dawah, H.A., Wilson, M.R. (Ed.),
(1997). Species: The Units of Biodiversity. Chapman & Hall, London
Majerus, M., Amos, W., Hurst, G., (1996). Evolution: The Four Billion Year War. Longman,
Harlow.
Mallet, J., (1995). A species definition for the Modern Synthesis. TREE. 10(7): 294-299.
Mayr, E., (1942). Systematics and the origin of species. Columbia University Press, New York. In
Majerus, M., Amos, W., Hurst, G., (1996). Evolution: The Four Billion Year War. Longman,
Harlow.
Palumbi, S.R., (1992). Marine Speciation on a small planet. TREE. 7(10): 114-118.
Paterson, H.E.H., (1981). Evolution and the Recognition Concept of Species: Collected Writings.
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Word Count = 2664 (inc. References)
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