Evolution and speciation in the Bahamian land snail Cerion

Cerion, the most variable and difficult genus of land snails to classify, have been the focus of a yet to be completed collaborative study by Stephen Jay Gould (Harvard) and myself spanning 25 years. My examination of geographic patterns of allozymic variation enabled us to resolve the evolution of these enigmatic animals and define their biological species in terms of covariation of genetic, phenetic and biogeographic traits. My work on the genodynamics of hybrid zones was published prominently and led to the discovery of a new class of allelic protein variants called hybrizymes that have since been the subject of molecular genetic doctoral studies elsewhere.

West Indian land snails of the genus Cerion are extraordinarily variable and over 600 species have been described in the past on the basis of shell form. Their conchological variability and chaotic pattern of distribution in the Bahamas and Cuba have frustrated the greatest malacologists (Bill Clench regarded them as the most difficult group of pulmonate snails to classify) and evolutionary biologists (Ernst Mayr despaired at applying the biological species concept to the group). Using a combination of field and laboratory techniques, Stephen Jay Gould and I showed that most of these species are invalid and are in the process of revising the genus. Our approach was systematic and biogeographic and, to date, we have completed fieldwork on all major islands in the Bahamas and completed monographs for four island banks. In addition, Cerion provide outstanding material with which to examine such important general problems as the role of differential growth rates in phenotypic evolution, and the significance of hybridization in natural populations and anastamosis in phylogeny.

My collaboration with Gould was remarkable in its duration and productivity. When we were first introduced to one another neither of us was aware that the other had begun to work on the same group; Gould on fossils and I on the ecology and genetics of living snails. Gould and I shared the field work and writing of our papers equally. I carried out the genetic analyses and Gould measured the shells and analyzed the morphometric data. Although our personal research efforts diverged since NSF-funding ceased in 1988 (after 15 years of support) we continued to work up our back-log of manuscripts at a rate of 1–2 each year until Gould died in 2002. Since then progress on my completion of our monograph of the Cerion of Great Inagua has been frustrated by the disappearance of Gould’s field notebooks and our annotated maps.

Our joint research on Cerion has resulted in 14 papers so far, not counting Gould’s own papers and the publications by others that it has stimulated. I was originally attracted to Cerion as a model system for the investigation of hybrid zones, an extension of my dissertation work on Pseudophryne to an animal that was much easier to study. Three particularly significant papers on Cerion hybrid zones are:

  • Publication 58 on the genodynamics of hybrid zones appeared in the festschrift Essays on Evolution and Speciation in Honor of M. J. D. White that I conceived and edited.
  • Publication 84, in the journal Evolution, reports an analysis of 50 years of interspecific hybridization in Florida.
  • Publication 98, in the Biological Journal of the Linnean Society, describes genetic anomalies associated with Cerion hybrid zones and introduces a new class of electromorphic variants for which I coined the term hybrizymes.
  • These papers addressed issues of great generality and have been cited in numerous studies of other organisms.

Our three most significant co-authored papers on broader aspects of the evolution of these remarkable snails are:

  • Publication 60 on geographic differentiation and speciation lays out our breakthrough re-interpretation of the Cerion’s evolution.
  • Publication 74 employs those insights in the context of a radical revision of the Cerion on one small island; 93 species-level taxa are shown to be referable to two semispecies and a phantom (a species present in the past but hybridized out of existence).
  • Publication 110 comprises a major review of the idea that history is the most significant cause of Area Effects with an illustration from Cerion on Great Inagua, Bahamas.

Phenotypic variation of Cerion illustrated by average specimens of 13 species. Seven species in the lower row are parapatrically distributed on a single island: Long Island, Bahamas. See Publication 46: Fig. 1 for details and size bar.

Publications

27. Gould, S.J., D.S. Woodruff and J.P. Martin. Genetics and morphometrics of Cerion at Pongo Carpet: A new systematic approach to this enigmatic land snail. Systematic Zoology 23:518–535. (1975a).
Note: Cerion are famous for their exuberant morphological variability. Over 600 species have been described based on shell variation. This is the first of a series of papers where Gould and I provide an evolutionary solution to this taxonomic nightmare. Here, in a study of one conchologically divergent population, we demonstrated that a combination of morphometric, genetic and biogeographic data revealed, for the first time, coherent patterns of variation. Gould and Woodruff shared the field work and writing equally. Woodruff carried out the genetic analyses. Undergraduate student, Martin, measured the shells and Gould analyzed the morphometric data. [No. of citations: 46]

28. Woodruff, D.S. A new approach to the systematics and ecology of the genus Cerion. Malacological Review 8(1):128. (1975b). [No. of ISI citations: 3]

29. Woodruff, D.S. Natural History of Cerion V. Allozyme variation and genic heterozygosity in the Bahaman pulmonate Cerion bendalli. Malacological Review 8(1):47–55. (1975c).
Note: I described the allozyme methods used in the Cerion project. [No. of ISI citations: 15]

44. Gould, S.J. and D.S. Woodruff. Natural History of Cerion VIII: Little Bahama Bank – A revision based on genetics, morphometrics and geographical distribution. Bulletin of the Museum of Comparative Zoology 148:371–415. (1978b).
Note: Monograph resolving apparently chaotic patterns of conchological variation and taxonomy on an entire island bank in the northern Bahamas. We also provided the first detailed description of a Cerion hybrid zone. Gould and Woodruff shared the field work and writing equally. Woodruff carried out the genetics and Gould the morphometric analyses [No. of citations: 39]

46. Woodruff, D.S. Evolution and adaptive radiation of Cerion: A remarkably diverse group of West Indian land snails. Malacologia 17(2):223–239. (1978d).
Note: A description of the results of 5 years of personal observations on natural history, ecology, behavior and conchological variation. I reported some results of my experiments in which I individually marked about 1000 snails in two populations adjacent to a hybrid zone and monitored their movements to estimate longevity and gene flow. [No. of citations: 29]

58. Woodruff, D.S. Towards a genodynamics of hybrid zones: Studies of Australian frogs and West Indian land snails. In: Essays on Evolution and Speciation in Honor of M. J. D. White. Atchley, W.R. and D.S. Woodruff, eds. Cambridge University Press, Cambridge and New York, pp. 171–197. (1981a).
Note: Bill Atchley organized and I edited this Festschrift for our former mentor at the University of Melbourne and I presented a detailed description of several hybrid zones showing that genetic asymmetries in Cerion zones were understandable in terms of differential gene flow but that the apparent asymmetries in Pseudophryne zones may be artifacts of sampling. [No. of citations: 48]

59. Atchley, W.R. and D.S. Woodruff, editors. Evolution and Speciation: Essays in Honor of M.J.D. White. Cambridge University Press, Cambridge and New York, pp. ix+436. (1981b).
Note: Book reprinted by CUP in 2010 as publication 225. No. of citations: 38.

60. Woodruff, D.S. and S.J. Gould. Geographic differentiation and speciation in Cerion: A preliminary discussion of patterns and processes. Biological Journal of the Linnean Society 14:389–416. (1981c).
Note: Major contribution showing how chaotic patterns of geographic variation, that had confounded interpretation for a century, could be resolved using a combination of morphometric, genetic and biogeographic data. Gould and Woodruff shared the field work and writing equally. Woodruff carried out the genetics and Gould the morphometric analyses. [No. of citations: 39]

74. Gould, S.J. and D.S. Woodruff. Evolution and systematics of Cerion on New Providence Island – A radical revision. Bulletin of the American Museum of Natural History 182:389–490. (1986b).
Note: Monographic revision in which we show that an island with 93 putative species has actually two allopatrically distributed semispecies that hybridize today. More significantly, we discovered genetic and morphometric evidence of a third species (a phantom embedded within a contemporary species) which was introgressed out of existence on this island a century ago. [No. of citations: 39]

84. Woodruff, D.S. and S.J. Gould. Fifty years of interspecific hybridization: Genetics and morphometrics of a controlled experiment involving the land snail Cerion in Florida. Evolution 41:1022–1045. (1987c).
Note: I discovered descendents of a colony of snails translocated from the Bahamas to the Florida Keys in 1915 to test the Lamarckian hypothesis. We used them to document the rates of conchological and genetic introgression -- a common feature of Cerion's history. Gould and Woodruff shared the field work and writing equally. Woodruff carried out the genetics and Gould the morphometric analyses. [No. of citations: 39]

85. Gould, S.J. and D.S. Woodruff. Systematics and levels of covariation in Cerion in the Turks and Caicos Islands. Bulletin of the Museum of Comparative Zoology 151(6):321–363. (1987d).
Note: Monographic revision of the Cerion on the southern-most island bank. Gould and Woodruff shared the field work and writing equally. Woodruff carried out the genetics and Gould the morphometric analyses. [No. of citations: 13]

98. Woodruff, D.S. Genetic anomalies associated with Cerion hybrid zones: the origin and maintenance of new electromorphic variants called hybrizymes. Biological Journal of the Linnean Society 36:281–294. (1989a).
Note: I reported the discovery of a new class of allozymic variants in Cerion and shown them to be markers of interspecific hybridization. I further showed that these hybrizymes occurred in many other plants and animals where they had typically been ignored as non-informative “rare alleles”. [No. of citations: 93]

104. Booth, C.L., D.S. Woodruff and S.J. Gould. Lack of significant associations between allozyme heterozygosity and phenotypic traits in the land snail Cerion. Evolution 44(1):210–213. (1989g).
Note: It was widely accepted that there was typically a positive correlation between genetic variability and phenotypic traits associated with fitness. Graduate student, Carey Booth, and I re-analyzed some morphometric data and found that, contrary to the received dogma, the Cerion data show no such relationship. [No. of citations: 35]

110. Gould, S.J. and D.S. Woodruff. History as a cause of Area Effects: An illustration from Cerion on Great Inagua, Bahamas. Biological Journal of the Linnean Society 40:67–98. (1990e).
Note: This is our major review and re-explanation of the widely observed Area Effect phenomenon based on a detailed analysis of one situation we discovered in Cerion. Subsequently, radio-isotopic dating of fossil shells from this site by our collaborator, the late Glenn Goodfriend, confirmed our historical hypothesis. Gould and Woodruff shared the field work and writing equally. Woodruff carried out the genetics and Gould the morphometric analyses. [No. of citations: 38]

168. Quensen, J.F. and D.S. Woodruff. Associations between shell morphology and land crab predation in the land snail Cerion. Functional Ecology 11(4): 464–471. (1997g).
Note: I have begun to prepare parts of my graduate student’s unpublished 1981 thesis for publication. In this paper Quensen and I show that shell strength-related features are probably adaptations to land crab predation pressures. Two additional papers are in preparation: one manuscript involves the effects of shell pigmentation on crypsis and thermoregulation; the other shows how geographic variation in shell strength tracks land crab distribution and abundance. [No. of citations: 10]

Stephen Jay Gould (1941–2002) on Great Inagua Island. June 1978.