Passive Speciation: Regarding the Taxonomic “Boldness” of Collins (1991)
Not long ago, in an issue of Herpetological Review, Brian I. Crother (2014) published an article praising the insightful taxonomic “boldness” of the late Joseph Collins, whose rather sweeping proposals appeared in the pages of the same journal twenty-three years earlier (Collins 1991). Following the suggestions of Frost and Hillis (1990) in applying the Evolutionary Species Concept (EvSC) to herpetological classification, Collins proposed to summarily elevate a list of 55 subspecies of amphibians and reptiles to full species status, based primarily on their respective distributions.
Collins proposed that a diagnosable population of a species (as indicated by its subspecific recognition), coupled with a hiatus in distribution (between it and the remainder of its species) was indicative of divergent evolutionary paths and, consequently, that the disjunct population should be elevated to separate species status. This essentially involved automatically extending full species rank to diagnosable but very closely related isolated populations, regardless of whether such populations had evolved any intrinsic reproductive isolating mechanisms or not.
It may be argued that non-overlapping distributions (allopatry) constitute a de facto reproductive barrier, but even if this is conceded, such a barrier would be extrinsic to the organisms themselves, rather than a character evolved by the organisms to avoid interbreeding. Thus, we have a phenomenon that could be charitably described as “passive speciation,” in which the organisms themselves are involved in the speciation process hardly at all, the presumption being that their respective genes are randomly drifting or responding to localized selection without the mediating influence of exchange with conspecifics.
Ironically, Collins later (1992) contended that his proposal was a more “conservative” option than continuing to regard such isolated populations as belonging to the same species as their disjunct kin—albeit as subspecies. It was perhaps conservative in a procedural sense, but hardly so with respect to the number of species being proposed while discounting the overwhelming phenotypic similarity of the taxa involved. The traditional (i.e., “conservative”) approach had been that, in the absence of demonstrable evidence of intergradation, similar but disjunct taxa be regarded as full species. The great rattlesnake systematist, L. M. Klauber, wrestled with this question with respect to island forms when writing his 1956 treatise:
I have been somewhat inconsistent in the treatment of island forms. Many taxonomists adhere to the strictly objective and easily applied rule that a subspecific designation must involve the actuality, or at least the possibility, of existing intergradations, which most island forms clearly lack. But consistently to apply this rule causes a loss in the value of nomenclature, insofar as the latter can indicate relationships. Thus, for example, if the island form estebanensis is considered a full species, its name will indicate no closer relationship to molossus than to atrox or mitchelli. Yet its derivation from molossus is so evident, and the extent of its divergence from molossus so moderate, that the adoption of the subspecific name C. molossus estebanensis has a real practical value. So, in assigning the names of island subspecies, I have been guided, not by the possibility of intergradations, of which clearly there is none, but by the extent of the divergence from the mainland form. . . .
In the case of some Mexican and other mainland forms, of which adequate collections are not at hand, I have adopted subspecific relationships where such are indicated, even though the lack of specimens from critical intermediate areas leaves intergradations unproved. Again, this has been done for the purpose of indicating probable relationships. (Klauber 1956)
Consequently, increasing the total number of species units without any concrete evidence that a physical, organic speciation event inherent in the organisms themselves had occurred hardly seems “conservative”.
It is noteworthy that Collins’ taxonomic proposals were not the result of any actual study of the taxa involved on his part; he merely consulted the range maps in the Houghton Mifflin field guides seeking out isolated subspecies. He was, in effect, applying his preferred species concept to the “problem” of disjunct subspecies. The EvSC does not require the existence of any sort of reproductive incompatibility (other than that passively imposed by allopatry) to bestow full species status upon putative diverging populations (increasingly, still more radical phylogenetic species concepts have even dispensed with the allopatry requirement, recognizing even parapatric populations with “hybrid zones” as discrete species).
Ernst Mayr, the founder of the Biological Species Concept (BSC), which Collins and most “modern” herpetological phylogeneticists remarkably consider “out-dated,” was unequivocal concerning the necessity for reproductive isolation in his concept:
Isolating mechanisms are biological properties of individuals which prevent the interbreeding of populations that are actually or potentially sympatric. This definition clearly excludes geographic isolation. . . . Isolating mechanisms always have a partially genetic basis. (Mayr 1963).
Somewhat paradoxically, even the species concept based on cladistic analysis devised by Willi Hennig (1950, 1966), the Hennigian Species Concept (HSC), also has an absolute requirement for reproductive isolation between putative species. This is paradoxical mainly because most current proponents of the EvSC are also devout Hennigians (i.e., cladists) in their preferred methods of determining phylogenies. In defending the Hennigian Species Concept, Rudolf Meier and Ranier Willmann (2000) make the following points concerning reproductive isolation with respect to speciation:
We believe that absolute reproductive isolation is this criterion [for determining speciation]. Its occurrence is a point of no return in the evolutionary process and keeps natural groups of populations apart. . . . Isolation mechanisms are intrinsic to the organisms involved, whereas geophysical obstacles are not isolation mechanisms but cause the mere (geographic) separation. Therefore, our discussion of isolation mechanisms never refers to separation. To borrow an example . . . , just because a few deer are kept in the basement of the American Museum, they are not reproductively isolated but merely separated. They are not a new species. . . . Given that the deer . . . are a family group, they probably have some unique genetic markers and would probably constitute [a] phylogenetic species [under some phylogenetic species concepts]. (Meier and Willmann 2000).
As to whether Collins' proposals have stood the test of time, as Crother claims most of them that have been examined have: well, yes and no. It depends entirely on which species concept one applies. If the EvSC is applied, as Collins preferred, then the answer is yes. But under the, I would say more rigorous and truly conservative BSC, then no.
Collins, Joseph. 1991. Viewpoint: A new taxonomic arrangement for some North American amphibians and reptiles. Herpetol. Rev. 22(2): 42-43
_____________. 1992. The Evolutionary Species Concept: A Reply To Van Devender et al. and Montanucci. Herpetological Review 23(2): 43-46
Crother, Brian I. 2014. The Bold Taxonomic Hypotheses of Collins (1991): 23 Years Later. Herpetol. Rev. 45(2): 268-272
Frost, D.R., and D.M. Hillis. 1990. Species in concept and practice: herpetological applications. Herpetologica 46(1): 87-104
Hennig, W. 1950. Grundzüge einer Theorie der phylogenetischen Systematik. Berlin: Aufbau.
_________. 1966. Phylogenetic Systematics. Urbana, IL: Univ. of Illinois Press.
Klauber, L.M. 1956. Rattlesnakes, their habits, life histories, and influence on mankind. 2 vols. Berkeley: University of California Press.
Mayr, E. 1963. Animal Species and Evolution. Cambridge: Belknap Press.
Meier, R. and R. Willmann. 2000. A Defense of the Hennigian Species Concept. In Wheeler, Q. D. and R. Meier (eds.). 2000. Species Concepts and Phylogenetic Theory: A Debate. New York: Columbia University Press
[This article appeared in the Fall 2018 edition of the SWCHR Bulletin.]