History As a Cause of Area Effects: an Illustration from Cerion on Great Inagua, Bahamas

Biological Journal ofthe Linnean Society (1990), 40: 67-98. With 10 figures History as a cause of area effects: an illustration from Cerion on Great Inagua, Bahamas STEPHEN JAY GOULD Museum of Comparative <oology, Harvard University, Cambridge, Massachusetts 02138, U.S.A. AND DAVID S. WOODRUFF Department of Biology C-016, University of California, San Diego, La Jolla, Callfornia 92093, U.S.A. Received 3 February 1989, accepted for publication 31 August 1989 The two parts of this paper work towards the common aim of setting contexts for and documenting explanations based on historical contingencies. The first part is a review of area effects in Cepaea. We discuss the original definitions and explanations, emphasizing the debate of adaptationist us. stochastic approaches, but arguing that the contrast of historical contingency us. selective fit to environment forms a more fruitful and fundamental context in discussing the origin of area effects. We argue that contingencies of bottlenecks and opening of formerly unsuited habitats may explain the classic area effects of Cepaea better than selectionist accounts originally proposed. The second part is a documentation of an area effect within Cerion columna on the northern coast of Great Inagua, Bahamas. Historical explanations are often plagued by insufficiency of preserved information, but the Inagua example provides an unusual density of data, with several independent criteria all pointing to the same conclusion. Shells in the area effect are squat and flat-topped in contrast with typical populations of long, thin, tapering shells living both east and west of the area effect. The flat-topped area effect is a result of introgression with a propagule of the C. dimidiatum stock (living on nearby Cuba, and most apically flattened of all Cerion). Fossils of this propagule were found fully cemented into highly indurated fossil soil crusts within the region of the current area effect. Multivariate morphometry, based on complex patterns of covariation, not just intermediacy in single characters, identifies the area effect samples as hybrids between this propagule and typical C. columna. Genetic analysis has identified three unexpected alleles in area effect samples only, and in no other snails of any other Cen‘on taxon anywhere else on Inagua. We hypothesize that the flat- topped area effect did not arise as a selective response to local environments within C. columna, but by introgression from a fortuitously introduced propagule of the C. dimidialum complex. The unexpected alleles therefore represent genetic phantoms of C. dimidiafum’s former presence or are hybrizymes-novel alleles produced by interspecific hybridization. CONTENTS I. Area effects in nature and literature . , . 68 11. Area effects in Cerion . , . , . 75 111. The flat-topped area effect in C. columna of Great Inagua . 78 67 0024-4066/90/050067 + 32 $03.00/0 0 1990 The Linnean Society of London 68 S. J. COULD AND D. S. WOODRUFF IV. Morphometrics of the area effect ..............85 (A) Material and methods. ...............85 (B) Distinctness of the area effect and its production by covariance ......85 (C) The founding propagule as a morphogenetic source ........88 (D) Discreteness of the morphological area effect ..........91 V. Genetics and the area effect. ...............92 VI. Conclusion: on the power of history .............95 Acknowledgements ..................96 References. .................... 96 I. AREA EFFECTS IN NATURE AND LITERATURE Committed as we are to understanding the general processes of evolution, and delighting as we do in nature’s diversity, nothing can be quite so satisfying to an evolutionary biologist as the intersection of an organism with a problem. Thus, certain taxa become exemplars of particular issues: humans for the evolution of mentality, siphonophores for the meaning of individuality. In this set of intersections, land snails stand supreme for the study of diversity-expressed particularly as visible polymorphisms of colour banding-within species or local populations. Cepaea nemoralis, the European banded snail, is by no means the most polymorphic of species; yet, by virtue of location, it has become the chief bearer of these arguments-for Cepaea dwells (in profusion) in England, a land of ubiquitous gardens and idiosyncratic individualism. W. H. Hudson, greatest of all naturalist-writers, exclaimed ( 1900: 60) : “Everyone knows how extremely variable in colour the shell of this snail is; in every garden a pretty collection may be made of shells, red, yellow, cream, and brown of many shades; shells marked and unmarked, with great variety, too, in their markings”. The maintenance of so much visible diversity in single locations, combined with striking differentiation among adjacent populations living in apparently identical environments, led most early evolutionists to the conviction, contrary to the panselectionist hopes of Wallace (1889: 148) and Weismann, that these snails provided our best prima facie case for non-adaptive differences both within populations and in the process of speciation itself (Gulick, 1873, 1905; Crampton, 1917, 1932). Gulick even maintained, in his famous treatise on the Hawaiian achatinellids (see Provine, 1986 on its influence, particularly upon Sewall Wright) that such non-adaptive variation constituted proof of randomness, and by extension of human free will, against the heartless and deterministic forces of Darwinism. Even as natural selection regained its pride of place in the early days of the Modern Synthesis, all architects of this theory agreed that polymorphism in Cepaea provided a primary example of non-adaptive variation. Mayr (1942: 759) regarded Diver’s work (1940) as “convincing proof for the selective neutrality of the alternating characters”. Huxley stated that “the distribution of types appears to be wholly random” (1942: 161), while Haldane (1932: 174) calculated that any coefficient of selection on banding alleles would be lop5 or less, in other words not intense enough to overcome either recurrent mutation or random drift. Dobzhansky (1937: 136), writing for Partula and Achatinella in particular, but denoting Cepaea by extension as well, wrote: “It seems impossible to establish any connection between the characteristics of the race inhabiting a given valley and the environment predominant in the valley. It is likewise AREA EFFECTS AND CERIOX 69 impossible to ascribe any adaptive significance to the peculiarities distinguishing the races from one another”. A theory triumphs best when it manages to resolve into its orbit the most powerful of apparent exceptions. Thus, the elegant work of Cain & Sheppard (1950, 1952, 1954) on determination of morph frequencies by selection for crypsis in local habitats (against visual predation by thrushes) unleashed a flood of reinterpretation in selectionist terms. As the modern synthesis ‘hardened’ (Gould, 1983) in its increasing reliance upon selection and relegation of non- adaptive effects to a periphery of unimportance, a flood of cepaeological works, particularly from the British school of ecological genetics, detected adaptation on a multiplicity of bases-against predators, to climate, for frequency dependence (see reviews of Jones, Leith & Rawlings, 1977 and Clarke et al., 1978; these articles also allow a much reduced role for random processes). So effective was this reinterpretation that Lewontin could write in 1974 (p. 234): “The case of Cepaea is regarded as a paradigm by selectionists”. And Mayr could even proclaim (1970: 2, 122): “Selective neutrality can be excluded almost automatically wherever polymorphism or character clines (gradients) are found in natural populations”. But conceptual transformations are seldom so unambiguous, and the selectionist reinterpretation of Cepaea encountered its paramount obstacle in the discovery of so-called ‘area effects’ by Cain & Currey (1963a). At lower elevations, in the variegated habitats of hedgerows, fields and beechwoods, morph frequencies in colonies of Cepaea did match their backgrounds, as the selectionist interpretation predicted. But in the higher grasslands of the English chalk downs, Cain & Currey found areas of diverse habitat, far larger than the panmictic unit of Cepaea, yet inhabited by populations of unvarying morph frequencies. Moreover, these areas of unvarying phenotype yielded to regions of equally stable, but different, forms along sharp clinal boundaries bearing no apparent relationship to any aspect of habitat or background. It seemed that morph frequencies were correlating primarily with location, rather than habitat as the selectionist interpretation required. Cain & Currey therefore referred to these regions of geographic constancy over varying environments as ‘area effects’. Their original definition reads: The predominance of a few morphs irrespective of habitat and background characterizes areas vastly larger than that of a panmictic population. Such a constancy of morph frequencies over a large and diverse area in spite of visual selection we call an area effect (1963a: 2). The concept has since been taken up within the larger body of evolutionary theory (White, 1978; Wright, 1965, 1978) and generalized (see Goodhart, 1987; 49, for example) to encompass populations in regions much larger than panmictic units that usually grade to others across sharp clinal borders, and that maintain distinctive and constant features of morphology or genetics within a region of varied habitat that might be expected to exert selection for local

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