S26.3: Species as multifaceted entities

A conceptually sound and empirically useful species concept is essential to both descriptive and comparative biology (Zink 1997) and for the effective conservation of biodiversity (Rojas 1992; Crowe 1993; Collar 1997). Up until the early 1980s, it was generally accepted amongst ornithologists that Ernst Mayr (1942) had provided just such a concept, the Biological Species Concept (BSC), and that its application had led to the discovery of all but a ‘handful’ of extant bird species (Farner & King 1971: xiii). According to the BSC, species among sexual organisms are real, self-defining entities (Clancey 1992) whose outer taxonomic limits are set at the level at which completely successful reproduction occurs, or is inferred to occur (i.e. resulting in the production of offspring which, in turn, reproduce successfully) (Mayr 1942). Other taxa, e.g. subspecies, genera, tribes, etc., are merely products of taxonomic ‘opinion’ or ‘convenience’ (Clancey 1992: 73).

There is by no means complete consensus as to just what constitutes a species amongst advocates of reproduction-based species concepts. Some proponents of the BSC maintain that reproductive isolation is a necessary, but not sufficient, condition for 'complete' speciation and consider species as potentially less inclusive entities. Bock (1992), for example, maintains that ecological compatibility in sympatry between putative species is an additional criterion for complete speciation. Paterson (1985), an advocate of another reproduction-based species concept (the Recognition Concept), considers sexual species as potentially more inclusive entities, expanding their membership to the limits at which mates unpremeditatedly 'recognise' one another as suitable sexual partners, regardless of the success of any reproductive attempt or act.

Since the early 1980s, there has been a range of challenges to reproduction-based species concepts. These challenges are based primarily on the premise that the application of these concepts can cause both taxonomic and phylogenetic errors. With regard to the former, they fail to recognise the full complement of taxonomically diagnosable units/products of evolution (Cracraft 1983, 1989; Zink 1997). With regard to the latter, setting the outer limits of species taxa to those of reproductive compatibility can result in hypotheses of monophyly for phylogenetically unresolved sets of para- or polyphyletic taxa (Cracraft 1983, 1989; Zink 1997).

In order to avoid these two classes of errors, a range of systematists have proposed alternative, phylogenetically compatible species concepts (PSCs) that are not so prone to these errors (e.g. Cracraft 1983, 1989; McKitrick & Zink 1988; Nixon & Wheeler 1990; Wheeler & Nixon 1990; de Queiroz and Donoghue 1988, 1990; Vrana & Wheeler 1992). Although all of these concepts assume that reproductive compatibility is necessary for the conspecificity of sexual organisms, none consider it to be a sufficient criterion for setting the upper taxonomic limits of species. These limits are set rather according to the criterion of taxonomic diagnosability.

The primary differences among the various PSCs relate to what constitutes a sufficient taxonomic diagnosis and what is the least inclusive taxonomic category that may be employed (i.e. species vs subspecies and varieties). Perhaps the most radical version of the PSC is that of Vrana and Wheeler (1992) who maintain that species are the least inclusive products of phylogenetic analysis. In the extreme, these can be individual organisms which may be diagnosed, for example, by the sharing of tiny bits of similar, non-coding DNA regardless of the nature of inter-individual relationships of parental pattern of ancestry and descent. Moving up one level is Cracraft (1983, 1989) who requires a species to be at least a diagnosable cluster of individuals linked by a parental pattern of ancestry and descent. However, he does not employ subspecies to describe variation among or within such clusters (Cracraft 1992). Although I advocate the use of a PSC (Crowe 1993), I employ the subspecies category based on quantitative/qualitative, geographically congruent character variation (Crowe 1978) to identify diagnosable taxa between which there is apparently unrestricted interbreeding in areas of extensive para or sympatry.

More inclusive further still are Nixon & Wheeler (1990) and Wheeler & Nixon (1990) who stipulate that species should be aggregations of populations (of sexual individuals) or lineages (of asexual individuals) of comparable sex/life stages (semaphoronts). Donoghue (1985) will even accept phylogenetically unresolved taxonomic units (metaspecies) as species provided that they are hypothesised to be a sister to one that is demonstrably monophyletic. The most conservative PSC advocates (e.g. Rosen 1979) require species to be monophyletic groups defined by one or more unique, derived features, i.e. autapomorphic species.

There is a further lack of consensus among supporters of PSCs as to the roles that evolutionary and ecological processes are allowed to enter into consideration when delimiting species. Most PSC-advocates eschew the role of processes in systematics: ‘Theory cannot be preferred over data’ (Vrana & Wheeler 1992: 69). However, Kluge (1990) sees a role for a fundamental historical process, descent with modification, and does not accept smallest phylogenetically diagnosable entities as species. He maintains (1990: 423) that ‘quality and amount of evidence must also be taken into consideration’ and argues that species are ‘historical individuals’ which are products, i.e. effects (not effecters) of the process of evolution. Individuals, demes and populations are merely ephemeral players on the evolutionary stage. It is terminal taxa that are the permanent products of evolution. But how, in practice, does one identify terminal taxa?

With the advent of multivariate statistical (Sneath & Sokal 1973; Bookstein 1992) and high-resolution molecular (Avise & Ball 1990) approaches to systematics, it is now possible to diagnose virtually every individual organism. So, what in practice should an ornithologist accept as necessary and sufficient taxonomic diagnosis of a terminal taxon? My aim in this brief report is to provide a personal, multifaceted solution to the species 'problem' by reviewing empirical taxonomic research conducted on African birds by myself and collaborators.

The word minimum can mean different things in different biological contexts. If the goal is to identify an alleged murderer or an unwilling parent, then the individual organism is the minimal unit of choice. However, if the goal is to identify terminal taxa, then we are seeking the least inclusive, potentially biologically meaningful, self-perpetuating, evolutionarily significant products of evolution. For comparative biological analysis or conservation action, a diagnosable cluster of individuals within a population of sexual organisms may not be an appropriate taxonomic unit. For such purposes, it is a population which can be diagnosed according to the possession of more than one character, not traits, which remains essentially invariant within, and 100% different between, demographically equivalent entities (Nixon & Wheeler 1990; Barrowclough 1992).

Defining a multifaceted species requires convincing evidence of a solid taxic diagnosis, i.e. congruent variation within and between populations for two or (preferably) more characters derived from effectively independent sectors of the genome. This follows what William Whewell termed a ‘consilience of inductions’ (see Ruse 1979). The greater the number of characters, the larger their coverage of the genome, and the more precise the congruence, the better the diagnosis. In other words, the presence of character A is highly predictive of the presence of character B, and so on: ‘if it walks like a duck, quacks like a duck, has webbed feet like a duck’, it must indeed be a duck’. From a taxonomic perspective such a character-consilience is geographically congruent variation in morphology, behaviour, molecular composition, etc. What is not a sufficient taxonomic diagnosis of a species is a difference in a single, apparently biologically insignificant, character (Wilson & Brown 1953), or less than precise congruence among a series of potentially genetically linked characters, in marked conflict with variation in other characters (Crowe 1978). An apparent taxic diagnosis based on one source of data (e.g. a chunk of non-coding DNA) within or between populations connected by gene flow can be dampened by back-mutation or interbreeding between para- or sympatric members of such 'clusters'. This could prevent the development of evolutionarily significant products (Avise & Ball 1990).

Nevertheless, despite such interbreeding, there are still taxonomically diagnosable entities connected by sometimes quite broad reproductive suture zones within which apparently unrestricted interbreeding may occur. Furthermore, some of these suture zones seem to have been geographically stable over time (Crowe 1978; Zink & Remsen 1983).

The Black Korhaan Eupoditis afra was considered to be a single, polytypic species comprising two or three subspecies (Sclater 1924) with only one character qualitatively distinguishing taxa within this assemblage (the amount of white on the wings). Furthermore, in the only area of parapatry between black and white-winged forms, there was evidence of interbreeding (D.G. Allan unpubl. data). Closer inspection, however, demonstrated the precise taxonomic and geographical congruence of a range of molecular (mitochondrial restriction fragment length polymorphisms), behavioural (calls and territorial displays) and morphometric (e.g. step-clinal variation in wing length) characters with wing colour and that the reproductive suture zone connecting these two congruently distinct forms was very narrow (<30 km) Crowe et al. (1994a). Therefore, two species are clearly warranted in this situation.

The taxonomic history of the Karoo Lark Certhilauda albescens is somewhat more complex. Depending on how somewhat congruent variation in plumage and morphometrics was interpreted, it has been split into as many as two genera, six species and seven subspecies (Roberts 1940). At the other extreme, its various taxa were lumped into a single, polytypic species (Clancey 1989). However, when vocal and molecular characters were added into the analysis, four multifaceted species emerged (Crowe et al. 1994b; Ryan et al. 1998). Six to 10 other clusters of populations which differed (but not precisely congruently) in plumage, morphometrics, song, and/or molecular characters, and which were observed to associate apparently randomly in parapatry were relegated the status of subspecies (Crowe et al. 1994b; Ryan & Bloomer 1997; Ryan et al. 1998).

Similarly, the Helmeted Guineafowl Numida meleagris, exhibits striking geographical variation in feather and other integumentary characters restricted largely to the head and neck (Crowe 1978). This variation shows some congruence with morphometric characters (Crowe 1978, 1979). However, there are reproductive suture zones, in some cases hundreds of kilometers in extent, linking all of its parapatric, taxonomically diagnosable forms. Within such zones, otherwise qualitatively distinct characters show a full range of intermediate conditions that are not geographically congruent. For these reasons, I relegated the nine taxonomically distinct forms of this guineafowl to the status of subspecies (Crowe 1978). However, preliminary results based on sequences of D-loop from mitochondrial DNA, which are congruent with the abovementioned characters, suggest that sets of these subspecies could be grouped into at least three phylogenetic species (P. Bloomer, Z. Rossouw & T.M. Crowe unpubl.).

To close this section, I would like to address the fears expressed by Avise & Ball (1990) and Collar (1997) that the inclusion of molecular information in species diagnoses will produce a glut of new 'trivial' species. My experience to date is exactly the opposite. Analyses of even the relatively taxonomically sensitive sources of molecular data we have investigated (sequences from D-loop of mitochondrial DNA) have not supported the recognition of more taxa than might be inferred from organismal characters.

Although my friend and co-convener of this symposium disagrees (Zink 1997), I maintain that the subspecies category may be the key to solving the species 'problem'. First and foremost, our non-systematist comparative biologists and the public in general must understand that our knowledge of avian taxonomy and phylogenetics is still far from complete. The ‘finality or stability’ that Collar (1997: 130) cries out for is simply not there. Moreover, species cannot always be delineated unambiguously and the goals of 100% diagnosability and precise character congruence are not always achieved. Therefore, just as ecologists and physiologists have recourse to measures of variance within which they can couch their conclusions, taxonomists should be allowed to use the subspecies category to state that: ‘This is a taxonomically diagnosable, phylogenetically compatible taxon but, for various reasons, I think that it should not be accorded the status of species.’ Valid reasons for not conferring species status are the presence of broad reproductive suture zones between entities, even when they are 100% diagnosable when comparisons are restricted to distally distributed populations (e.g. between the various forms of Helmeted Guineafowl and some of the forms of Karoo Lark) and, quite simply, a paucity of congruent evidence. Like it or not, there is still a crying need for competent taxonomists (Collar 1997) and good taxonomic characters.

Species are not special, self-defining taxa. They are discovered, just like other taxa, by existence of congruent character variation. Using reproductive compatibility to set the upper taxonomic boundaries of species can create both taxonomic and phylogenetic confusion. The keys to avoiding this confusion are to implement phylogenetically compatible species and subspecies concepts based on multifaceted data.

My research has been supported over the years by the University of Cape Town, Foundation for Research Development and the Frank M. Chapman Fund. I thank Mark Cooper, Sioban Munro, Peter Ryan and Peter Linder for their constructive comments on drafts of this report.

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