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

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 differences. Area effects have a much longer history of recognition, at least in the anecdotal writings of naturalists. In Nature in Downland (1900), W. H. Hudson clearly described such a phenomenon (and in the ‘type locality’ at that) when he followed his statement about diversity in gardens with this description of Cepaea on the downs: “Now most of the shells I see on the downs are of one type; indeed 70 S. J. GOULD AND D. S. WOODRUFF you may in some parts search the furzy spots for miles without getting a snail of any other type”. Hudson also recognized that this unvarying form did not provide good protection from predators. He noted the conspicuous character of shells and even speculated that their resemblance “to a small portion of a highly- colored adder’s coil” might frighten predators (1900: 60)-but evidently to no effect, for “wherever there is a patch of furze there you will find the ‘thrushes’ anvil’, usually a flint half or nearly quite buried in the soil a few feet away from the bushes, and all round the anvil the turf is strewn with shattered shells”. Cain & Currey’s interpretation unleashed a flurry of further documentation and revised interpretation. No aspect of the natural history of Cepueu has received more attention since 1963, but no resolution has occurred. Cameron, Carter & Palles-Clark wrote in 1980 (p. 336): “Amongst several patterns of variation in the shell color and banding polymorphisms in the land snail genus Cepueu, the ‘area effects’ of Cain & Currey are the most enigmatic”. The external world surely possesses an objective reality, but our decision on how to parse nature into a set of named phenomena must be strongly linked to our conventional modes of thought. The designation of ‘area effects’ provides a striking example of a ‘concept-bound’ term. We must first ask why Cain & Currey chose to give this phenomenon a separate name at all? What could be more basic or ordinary in evolution-a science of genealogical descent after all-than organisms living contiguously and looking alike? Is an area effect any more than a microgeographic race with some interesting peculiarities? The answer, of course, lies with Cain & Currey’s expectations. They had broken the non-adaptationist hegemony over Cepaeu’s variation and had won this chief example of postulated randomness for the growing selectionist orthodoxy. Now they had discovered a challenge in correlation of form with geography rather than habitat-and they quite properly named their anomaly on the basic principle that exceptions must be treasured. Area effects thus entered the literature in the odd guise of a negatively-defined concept-failure to find correlation with selective factors of predation or physical environment. We treasure our exceptions (as the clichi: goes), but we also try to resolve them in favoured ways. Cain & Currey were confident that their area effects must be formed and maintained by selection. They presented several strong arguments against random processes. Populations are too large and their frequencies too constant; some area effects have been stable since Neolithic times (subfossil shells may retain their colour) ; agricultural and climatic history show no disturbance (ploughing or drought) sufficiently severe during the last 200 years to force populations through a bottleneck rendering them subject to random drift. Cain & Currey therefore returned to their selectionist preferences by eliminating alternatives. Yet they could find no positive evidence for an adaptive basis of area effects. They therefore conjectured that the effects were being maintained by environmental selection-and that the climatic agents were cryptic in expression (they tried to establish a relationship between brown colouration and the ponding of cold air, for example). “It seems clear”, they wrote, “that the area effects are caused by some form of selection, but the topography, geology, and vegetation of the Marlborough Downs gives no clue to what this could be for banding” (1963a: 2). They concluded more positively that “physiological selection, probably in relation to local climatic differences, may play the greater part in determining gene frequencies, to such an extent that AREA EFFECTS AND CERION 71 particular phenotypes may predominate greatly in particular areas” ( 1963a: 3). Putting a best face upon their failure to find direct evidence for selection, they concluded that selection might be very strong if it could produce such a profound effect without an evident expression. Area effects, they responded to a first challenge (Goodhart, 1963, see below), “point rather clearly to the existence of environmental selection. If, however, the existence of environmental selection not related to the obvious features of the environment is admitted, then for all we know, it may be extremely strong” (Cain & Currey, 1963b: 469). They concluded that “the interaction of selective forces is complex, and seems to leave little scope for purely random effects” (1963b: 271). Despite the failure of Cain & Currey to find direct evidence for environmental selection, their favoured explanation passed into textbook wisdom as a result (we must assume) of its congeniality with orthodox views, surely not on its basis in evidence! Ford (1964) simply stated that area effects record “physiological selection”; while Mayr (1970: 122) ascribed them to “highly localized selective factors”. But theories based on an absence of evidence and a call for cryptic causes do not go unchallenged. Goodhart (1963) was first to present an alternative based on founder effects and genetic coadaptation, an idea surely plausible but equally free of direct evidence. Goodhart argued that area effects might begin with initial stocks small enough for founder effects and random drift to be effective. As these non-adaptive forces cause populations to move to differing regions of an adaptive surface, selection will then draw them to different adaptive peaks. Each peak is an adequate solution, then strengthened and maintained through genetic coadaptation by the evolution of modifiers, but differences between peaks are ‘non-adaptive’-and Goodhart used this ‘inflammatory’ word in his title. Populations stabilize, expand and may eventually meet. Areas of contact may form sharp clines due to reduced hybrid viability between differently coadapted populations. Sewall Wright (1965, 1978) then became interested in area effects as a possible illustration of his shifting balance theory. He agreed with Goodhart about the efficacy of drift and the importance of coadaptation, but disagreed that area effects must represent populations that started out tiny and then expanded. He argued that populations might have been consistently large and widespread, but broken into semi-independent demes suitable for the operation of his shifting balance process. Thus, the sharp clines might have evolved in situ and not as zones of secondary contact. He wrote (1965: 102): Under my view, however, random processes followed by selection may have established a new favourable combination at a center within a population as large as at present and this combination may then have spread gradually over the observed large area, by small amounts of emigration and cross- breeding at each step. Bryan Clarke (1966) then developed his important theory for the evolution of morph-ratio clines, largely in response to the problem of area effects in Cepaea. He delineated situations in which selection can steepen clines in situ and produce the ‘area effect’ phenomenon of constancy within a region and sharp discontinuities between, without appealing “either to corresponding discontinuities of environmental factors, or to the founder principle” (1966: 30). These three types of explanation have dominated the discussion ever 72 S. J. GOULD AND D. S. WOODRUFF sinceimmediate selection by cryptic environmental factors (Cain & Currey), secondary contact following differences established by founder effects and subsequent genetic coadaptation (Goodhart), and differentiation within large populations, with random effects and coadaptation to initiate and maintain subregions at different adaptive peaks (Wright and Clarke). Interest in area effects became more general when Michael White (1978) proposed that they might represent incipient stages in a widespread process of parapatric speciation without major karyotypic change. (White titled chapter 5 of his book “Clinal and Area-Effect Speciation”. This suggestion has not been validated, and Cepaea itself has many area effects but only four species.) With this strong concern among so many leaders in evolutionary studies, area effects inevitably became a subject of general interest. Just as we parse nature in varying ways that depend upon our conceptual interests, so too can we construct allegiances among contrasting explanations in a variety of manners that reflect our dominant concerns; there is no one ‘correct’ framework for this debate. For example, if concern for the origin of sharp boundaries between area effects were paramount, then we might ally Cain and Currey with Clarke and Wright, since both schemes view the boundaries as developed in situ-in contrast with Goodhart’s interpretation of secondary contact. But the argument has usually been read in a different way because it intersects the oldest, perennially contentious, issue in evolutionary theory-random effects versus natural selection-and therefore becomes one more episode in this struggle. The evolutionary study of Cepaea was born and nurtured squarely within this debate (see above). The literature on area effects has therefore made a primary division between Cain & Currey as selectionists and both the Goodhart and the Wright-Clarke school as allowing a major role for genetic drift or founder effects. We believe that this largely false division has only sown further confusioa and impeded resolution by forcing protagonists to talk past each other. The problem, as so often (see Gould & Vrba, 1982)’ lies in the failure to distinguish historical origin from current utility (or reasons for maintenance). No one has challenged the assumption that selection now acts strongly in maintaining area effects. (The nature of selection remains at issue, with Cain & Currey advocating ordinary response to external factors of the environment, while Goodhart and Wright speak of an internal selection to strengthen and maintain coadaptation. Wright, for example (1978: 237, see also Goodhart, 1987: 330), states: “Area effects may thus be due quite as well to selection in relation to different internal environments (genetic backgrounds of the major genes under consideration) as to selection in relation to different external environments as assumed by Cain & Currey”. Yet Cain & Currey’s defence of selection has always rested upon arguments for maintenance-particularly the age of the effects and the continuously large populations (Currey & Cain, 1968: 3, for example)-a theme that Goodhart does not challenge, since his random forces only operate in setting the origin of area effects by permitting an exploration of various adaptive peaks. As an example, consider the argument of Jones et al. (1977: 130) against randomness based only upon current maintenance-a point that no one would rebut and that does not speak to either Goodhart’s or Wright’s alternative: “The stability of some area effects over thousands of years is also hard to explain unless they are actively maintained”. AREA EFFECTS AND CERZOX 73 We believe that this primary confusion could be resolved by recognizing that a related (but deeper and different) issue lies at the core of this traditional parsing between adaptive and random. (We do not, following our stricture above, argue that this conceptual scheme is either unique or more attuned to nature; we do say that it may be better in the sense of clarifying and ordering the issues that have concerned protagonists in this discussion. Intellectual life is largely the struggle to find fruitful contexts.) Consider the fact that precipitated this entire debate: area effects were born in an anomaly-a lack of concordance between phenotypic distribution and its surrounding environment and habitat. Basically, two kinds of solutions have been offered to explain this absence of apparent correlation. Cain & Currey argued that the concordance exists, but we have not yet identified the appropriate environmental factors. The other two schools claim that concordance truly does not exist because the area effect had its origin in a phenomenon of past history not reflected in the current selective forces of surrounding environments. (The fact that selection may now maintain one of a dozen once-possible peaks does not speak to our interest in why this particular peak exists here and now.) If an explanation of area effects requires a knowledge of past historical states (as in Goodhart’s and Wright’s invocation of random effects either in small founding populations or in semi-isolated demes that then spread by interdemic selection), then our search for causes must extend beyond an understanding of current circumstances, selective or otherwise. History becomes a necessary component in our explanation. The focal question of historical science is never ‘why this’-an issue that can usually be resolved, as for area effects, by the study of current forces. Our concern must be ‘why this and not another plausible and workable pathway’-a question that usually requires a knowledge of history’s contingencies. Surely no one will accept ‘it works’ as a resolution to the puzzle of why human intelligence evolved. Likewise, ‘it fits’ may not provide the answer to why we find area effects in Cepaea. This statement will suffice if Cain & Currey are right, but current fit will only solve a peripheral part of the puzzle if either of the other schools, which root their explanations for current states in past history, are correct. This issue of explanations rooted in history versus explanations based upon current utility lies at the heart of our recent debate about adaptation and constraint (Gould & Lewontin, 1979; Maynard Smith et al., 1985). Hardly any question in the historical sciences could be more important, and our field has often been hampered, particularly of late, by traditions that neglect or forget the dimension of history and try to view the current state of our evolved world as a problem in classical physics, with all components lying at optima directly controlled by current forces. We therefore contend that Cepaea’s area effects, and the history of debates about them, are not only best understood in the light of history versus current adaptation as a cause of particular phenotypes and their distribution, but also that a recasting of the debate into this context allies the subject of area effects with the most basic question in our field. In this light, we view most of the recent literature on area effects as offering striking support for the historical interpretation. Ochman, Jones & Selander (1983), for example, found three molecular area effects in Pyrrenean populations of Cepaea. These area effects correlate neither with colour phenotypes nor with 74 S. J. GOULD AND D. S. WOODRUFF major patterns of climate or vegetation. Ochman et al., interpret these area effects, and their sharp borders, as products of secondary contact among three populations that became small and isolated during the last glacial period, and then expanded while maintaining integrity at zones of meeting. They explicitly invoke the contrast of history and current causes by stating that the adaptive character of shell phenotypes (under selective control without area effects in this region) had ‘obscured’ the signs of past history now revealed in allozymic area effects. In a more telling defence of history-for it reinterprets the ‘type’ area effects first found by Cain & Currey on English downlands-Cameron and his colleagues have related the classic cases in Cepaea to reduction in populations caused by changing patterns of land use (Cameron & Dillon, 1984; Cameron et al., 1979, 1980). Perhaps there shall not always be an England, but that land does possess the virtues of relative stability and assiduous record keeping-the sine quibus non for any positive investigation of history. By studying such documents as late 18th century enclosure awards, mid 19th century tithe commutations, and ranging back as far as the Domesday Book and 10th century Saxon land charters, Cameron et al. (1980) have been able to establish a striking correlation: old and stable populations, on land in constant use for the same purposes during several centuries, do not show area effects, but do exhibit good correlation of morph frequencies to immediate pressures of selection. Area effects, by contrast, “are strongly associated with areas of habitat instability, where Cepaea survived as small and isolated populations until recently’’ ( 1980: 335). This correlation emphatically supports Goodhart’s notion that area effects record a history of previously reduced populations potentially subject to random effects, with later stabilization by coadaptation to one of many possible adaptive peaks. Cain & Currey (1963a) had recognized that such habitat instability might provide an explanation not based on current selection, and they did try to study patterns of land use, but Cameron et al. (1980) claim that Cain & Currey stressed the wrong factors of climate and agriculture. The answer, they hold, lies with sheep. As the ever-prescient W. H. Hudson noted, Cepaea does not live on heavily grazed land. (He wrote (Hudson, 1900) that Cepaea “is common everywhere in the furzy places, but is incapable of existence on the close-cropped turf’.) Until this century, high downland was used intensely as ‘sheepwalk’ (to cite a lovely word that is, itself, a historical vestige of a past and simpler way of life)-a practice now abandoned both because sheep raising has greatly declined and because remaining stocks are now kept at higher density on ‘improved’ grassland. After its abandonment as sheepwalk, the unploughable downlands became derelict and are now in succession to long grass, rough herbage and scrub-as congenial to Cepaea as the older grazed fields were not. “The habitats of Cepaea on downland at present . . . are thus of recent origin” (Cameron et al., 1980: 338). Over and over again, Cameron et al., have correlated area effects with regions only recently available for colonization. On the Salisbury Plain, area effects are “especially evident in just those places which were once sheepwalk” (1980: 354); the brown area effect of Fyfield Down covers a region that was “an actively managed rabbit warren subject to intense grazing pressure in the late 19th and early 20th centuries” (1980: 354). These reinterpretations have the salutary effect of enlarging the realm of AREA EFFECTS AND CERION 75 potential causes for area effects; they also supply a welcome corrective for a too- automatic reliance upon current selection as the agent of evolutionary pattern. But they also pose problems, two in particular. First, all area effects so far reinterpreted as products of history have been tied to one form of historical explanation: population bottlenecks and their attendant effects followed by later expansion and secondary contact with other populations. But history represents a class or category of explanations, not a particular scenario. Cameron & Dillon ( 1984), in offering their historical explanation for the classical area effects of Cepaea, clearly noted that they had made inferences for particular cases only, and that their proposed style of historical causation would not apply to all kinds of area effects. In particular, the classical Cepaea area effects are defined by features showing little covariation with other traits, even between phenotypes of linked loci. Other area effects, including the example from Cerion documented in part two of this paper, are defined by covariation of several independent traits. This covariation is consistent with the different kind of historical explanation, based on stabilization of hybrid populations, that we will propose for our Cerion area effect. We must be mindful of the caveat stated by Jones, Selander & Schnell (1980: 385): “The term ‘area effect’ should not be allowed to impose a spurious uniformity on a heterogeneous and poorly understood class of phenomena”. ’ Secondly, although history is pervasive, it remains frustrating in its difficulty of documentation. Speaking particularly of pulmonate studies, Jones ( 1980: 283) writes: “Historical effects are . . . notoriously difficult to assess . . . All theories of the origin of species depend on historical events which are by their nature not directly testable”. This dilemma has often led evolutionists to hope that they will not need history-for what good is a truth without potential evidence-and that the more easily validated forces of current selection will suffice. The only antidote to this problem is a search for those cases, admittedly rare, that preserve an adequate record of their past-either directly through fossils, or indirectly in inferences from present populations and their distribution. We write this paper because we have found an area effect within Cerion columna on the island of Great Inagua (Bahamas) that overcomes both these problems. Here we were fortunate enough to find evidence for a historical origin-both from direct evidence of fossils and indirect evidence of allozymes-based not upon small populations and later expansion, but upon in situ development following the arrival of a distant propagule from another species and its introgressive incorporation in the region of the area effect. This represents, we believe, the first documentation in pulmonates of an area effect developed in situ but not built by the selective advantage of its phenotype in the local environment.

11. AREA EFFECTS IN CERION Cerion, a West Indian land snail with centres of distribution in Cuba and the Bahama Islands (Clench, 1957; Gould & Woodruff, 1986; Woodruff & Gould, 1980), has long been noted and puzzled over by naturalists who have struggled to understand the basis for its unparalleled morphological variety-even among land molluscs, a group so well celebrated for diversity (Gulick, 1905; Crampton, 1917, 1932). Linnaeus named the type species (1758: 765), and Cerion has since 76 S. J. GOULD AND D. S. WOODRUFF commanded substantial career investments from some of our greatest evolutionary biologists (Mayr & Rosen, 1956; Mayr, 1963) and pulmonate taxonomists (Pilsbry & Vanatta, 1896; Bartsch, 1920; Clench, 1957). We have been studying Bahamian Cerion in the field, with subsequent morphometric and genetic studies of the same animals, for fifteen years (see reviews in Woodruff & Gould, 1980; Gould & Woodruff, 1986, 1987). Cerion forms numerous area effects within the geographic distribution of its species. These are not the continuous, gently clinal and ill-defined regional differences of conventional geographic variation, but true area effects as indicated by their distinctive constancy within regions (and across all habitats frequented by Cerion), and their sharp borders with neighbouring conspecific populations. Best demonstrated are the ‘Pongo Carpet’ variant within Cerion bendalli on Great Abaco (Gould, Woodruff & Martin, 1974), and the ribby area effects within C. malonei on Long Island (Woodruff & Gould, 1980). While we may suspect history on the negative evidence of no known environmental difference between area effects and adjacent regions, and on the failure of sharp phenotypic borders to correlate with any recognized discontinuity of habitat, we do not know how these area effects formed and persisted. Cerion does, however, manifest a biological peculiarity that provides, in principle, an easy, if unusual, pathway for the formation of area effects based on happenstances of history, rather than forces of local adaptation. Nearly all taxa of Cerion hybridize upon contact; we know only one unambiguous case of sympatry between two species (on Great Inagua, see Woodruff & Gould, 1980). These hybridizations cross all degrees of Cerion’s unrivalled morphological variation; they are not restricted to populations with similar phenotypes. Hybrid zones are not broad, smooth areas of insensible transition (these also occur aplenty within species of Cerion), but narrow zones of contact and instability, often accompanied by an explosion of phenotypic variation beyond the bounds of either parent (Gould & Woodruff, 1986; 435-440), and always marked by the presence of unexpected alleles (hybrizymes of Woodruff, 1989)-a phenomenon only recently discovered but already documented as taxonomically widespread and characteristic of hybrid zones (Sage & Selander, 1979; Barton & Hewitt, 1985; Hewitt, 1988). (We shall pursue no further here the vexatious question of what constitutes a species in Cerion. The argument of this paper only requires the established fact that distantly related populations within the genus will hybridize. We only wish to note that Cerion provides a classic example of a syngameon-a superspecies in which the component semispecies will hybridize, often without losing their integrity (Grant, 1971). Although evolutionary species concepts based on isolation or recognition appear inapplicable to Cerion the evolutionary cohesion species concept introduced by Templeton ( 1989) is well suited to dealing with this genus.) One other fact of Cerion’s biogeography sets the context for ‘accidental’ formation of area effects by hybridization. Most populations of Cerion are coastal in distribution and live on islands within a major hurricane belt. Transport of propagules by hurricanes (and other ‘rarely efficient’ means) has long been proposed as a major determinant of Cerion’s peculiar geographic distribution (Clench, 1957). This principle is documented for the subgenus C. (Umbonis)-a taxon that probably behaves no differently from others, but has the virtue of unambiguous recognition for its suite of unique and highly distinctive features AREA EFFECTS AND CERION 77

Figure 1. An area effect on North Andros Island, Bahamas. Top row: typical Cenon glans. Bottom row, shells of C.glans trregulare collected by the authors in 1982 1 km north of Nicholls Town. The wavy ribs and incised spiral lines of the area effect snails indicate introgression with a C. (Umbonu) propagule. The specimen top left is 25.8 mm in height.

(including wavy ribs, incised spiral lines, and its habit of incorporating sand grains within the shell, particularly at the adult aperture). Umbonis populations are scattered discontinuously and sporadically among Bahamian islands, but along hurricane tracks from a presumed Cuban source (Woodruff & Gould, 1980: 410). Umbonis usually hybridizes with local forms, and the resulting stabilized populations have often received distinctive names (C.feZis on Cat Island, C. bland on the Turks Islands.) 78 S. J. GOULD AND D. S. WOODRUFF Thus, a hurricane-borne propagule may land within the range of an indigenous Cerion species, hybridize in the region of its landfall and form within the distribution of the resident species a localized region of phenotypic and genetic peculiarity. If this deme forms no stable centre and grades broadly into neighbouring populations, it will only produce an odd hump in geographic variation. But if the hybrid population stabilizes, establishes its own integrity and spreads, forming sharp borders with neighbouring demes, it will form an area effect. Consider two examples of area effects originated by hybridization in Cerion. 1. North Andros. In 1907, L. Plate described C.glans irregulare as a peculiar geographic variant, with wavy ribs and an oddly triangular shape, within the standard ribby C. glans of Andros Island (Fig. 1). We visited Andros in 1982 and collected C. glans irregulare along its entire range. We found phenotypic stability throughout its 3.5 km of coastal residence (Morgan’s Bluff to Nicholls Town), and rapid transition to standard C. glans on either side. We also validated what we suspected about its origin: numerous specimens with incised spiral lines, incorporated sand grains, and other distinctive Umbonis characters, marked the origin of this area effect in hybridization between local C.glans and an immigrant propagule of C. (Umbonis). 2. Bahia Honda Key, Florida. Mimicking the process of natural transport, Bartsch transplanted a colony of Andros C. casablancae to Bahia Honda Key in 1912, an island within the range of C. incanum but then uninhabited by Cerion. Thanks to Bartsch’s unusually thorough documentation (see Woodruff & Gould, 1987), we know that C. incanum invaded the Key in 1928 and formed a hybrid population with this localized C. casablancae deme originated by only 55 individuals. This hybrid population, with its distinctive phenotype (Fig. 2), has thrived and spread over south-eastern Bahia Honda, forming an unexpectedly sharp morphological transition with normal C. incanum to the west (although genetic markers of C. casablancae extend farther into demes of pure C. incanum phenotype). While we do not doubt the formative role of fortuitous transport and hybridization in the origin of these area effects, neither case provides a fully satisfactory illustration for this historical style of explanation. The Florida example, though optimally documented, is only half a century old and may be evanescent (Bartsch’s first generation hybrids are closer to C. casablancae, while the current centroid has moved towards C. incanum). The Andros case spans at least 80 years, and may be much older, but we have no direct evidence for its origin. Ideally, we would like to find an example with both direct and indirect evidence, and old enough to show that area effects produced by hybridization can be stable at least for hundreds or thousands of years. We have found such a situation on Great Inagua.

111. ‘THE FLAT-TOPPED AREA EFFECT IN C. COLUMNA OF GREAT INAGUA Cerion faunas of the main Bahama Islands of Little and Great Bahama Bank are dominated by populations of the ribby and mottled morphotypes (see documentation and justification of terminology in Gould & Woodruff, 1978, 1986). However, islands of the south-eastern Bahamas have a different Cerion ‘signature’ in populations of the large, white, smooth-shelled, triangularly Figure 2. An area effect on Bahia Honda Key, Florida. Top row: Bartsch’s original specimens of C. casablancac, collected on South Andros and transplanted to Bahia Honda. Second row: hybrids collected by Baruch in 1933. Third row: phenotypes of the current area effect. The area effect of this hybrid phenotype maintains a sharp border to the west with typical C. incanurn. Fourth row: typical C. inconurn from western Bahia Honda Key. The specimen top left is 29.2 mm in height. 80 S. J. GOULD AND D. S. WOODRUFF

NORTH EAST POINT

DEMMAN’S BAY

~ ~~ Figure 3. The island of Great Inagua with inland lakes and salinas noted. Cerion colurnna ranges along the northern shore from Mutton Fish Point to south of Deadman’s Bay.

shaped phenotype that we have called the ‘tapering morphotype’ (Gould & Woodruff, 1987). These populations now bear different names on the various islands (most shall probably be synonymized), but each place has a representative. On Great Inagua (Fig. 3), populations of the tapering morphotype are called Cerion columna. They extend in a narrow strip along the northern coast of Inagua for a virtually unbroken run of 80 km from just west of Mutton Fish Point to the west (where we have documented a sharp hybrid transition to C. rubicundum, the dominant species on the rest of the island) to an unspecified region on the unexplored eastern coast between Deadman’s Bay where pure populations of C.columna have been collected, and Doghead Point where we have found C. rubicundum (see Fig. 3). (Cerion columna does not interbreed with dwarf C. rehderi, the third Inaguan species-this is the sole case of demonstrated sympatry in Cerion, as mentioned above.) Along this entire range, C. columna shows the continuously-graded, small-scale variation found within most species of Cerion-predominantly in ribbing and size (Fig. 4). However, when we reached the North Coast at Rocky Harbor in March 1980, an area previously uncollected due to difficulty of access, we found a unique and highly distinctive deme of C. columna, phenotypically far outside the range of all others. These shells (Fig. 5) have flattened tops, and squat, barrel- shaped profiles-thus directly flouting our designation of their morphotype as ‘tapering’. At first, we thought that we had discovered an odd ecophenotype or local adaptation, for our initial sample came from windswept coastal rocks (locality 892 of Fig. 6), and squat, quadrate shells seem to enhance stability in such environments. But we soon found that this peculiar shape characterized every AREA EFFECTS AND CERIOX 81

Figure 4. Geographic variation within C.columna. Left: large and smooth specimens from a population (our locality 852) west of the area effect. Middle: large and ribby population east of the area effect (MCZ collections). Right: small shelled sample east of the area effect (MCZ collections). The leftmost specimen is 40.6 mm in height. sample of Cerion columna within the region-across a full range of Cerion habitats from coastal rocks (892 and 894), to interior hilltops (897), to calm, sandy areas behind the hill (895). We then traced this phenotype westward and discovered a rapid transition to ordinary C. columna near the abandoned settlement of Babylon. We found intermediate populations at 898 and 899 (with the zone of intermediacy also spanning the entire geographic range of C. columna from coast to interior) and normal C. columna 500 m west at the western edge of the coastal pond (see Fig. 6). We did not trace this phenotype eastward, but typical C.columna has been collected at the long abandoned townsite of Lower Cockburn, 2 km east of Wilkes Hill. We know that C. columna is confined to a coastal strip here and elsewhere, for we traced this taxon through a hybrid zone into C. rubicundum to the south. Locality 900 has intermediates, while we find only C. rubicundum at 901 and 902, south of the line of lakes and salinas. This flat-topped phenotype forms a classical area effect in its distribution. Its size (3-5 km in coastal extent and about 750 m on average from coast to interior) greatly exceeds that of a panmictic unit in Cerion. Field studies of other species of Cerion have provided basic data on natural history, dispersal rates and effective neighbourhood size (Woodruff, unpublished; Woodruff & Gould, 1980). Cerion bendalli, for example, forms colonies on the order of lo3 adults occupying areas of 103m2.Within the colonies snails are clustered on a few plants and separated from adjacent colonies by distances of 2-3 times the diameter of the habitat patch (i.e. 20-30 m). Although individual snails have moved more than 82 S. J. GOULD AND D. S. WOODRUFF

Figure 5. Shells of the area effect contrasted with typical C. columna. Top: large area effect shells from the top of Wilkes Hill (locality 897). Middle: smaller shells of the area effect from coastal locality 892. Bottom: typical C. columna from locality 853. The top left specimen is 35.8 rnm in height. AREA EFFECTS AND CERfON 83

4” ROCKY HARBOUR

902 I KM 0 -

Figure 6. Map of the coastal region of the area effect. Salinas indicated by solid lines, topographic contourn (40 foot interval) by dotted lines. See text for details.

16 m yr-’ the mean displacement per 5-year generation was closer to 2 m and the maximum detected displacement over 10 years was 22m. We thus have a situation in Cerion where patchy distribution patterns coupled with extremely low vagility and small population size may permit a successful colonist to expand rapidly in a temporarily unoccupied area. This presumably happened on Great Inagua as the flat-topped phenotype occupies an area 2-3 orders of magnitude

Figure 7. Fossil shells (locality 893) of the C. dzmidzutum propagule. General width and flatness of apex are more extreme than in modern area effect shells. 84 S. J. GOULD AND D. S. WOODRUFF

Figure 8. A specimen from the fossil propagule imbedded in lithified soil crust to show that the degree of induration is anything but superficial. greater than the average neighbourhood size. The flat-topped phenotype is now stable within this region and present in all habitats. It maintains a sharp border, at least to the west, with conspecifics of ordinary form. With these data on modern phenotypes alone, we would have no relevant information about the cause of this area effect. However, a fortunate discovery has permitted us to resolve its origin (though we still have no information about forces of selection that may maintain and set its current distribution). In an intensely indurated fossil soil zone right at the region of the present area effect AREA EFFECTS AND CERION 85 (locality 893 of Fig. 6), we found fossils of a fully flat-topped Cerion (Figs 7, 8) indistinguishable from the Cuban species group of C. dimidiatum (a complex inhabiting the eastern area of Cuba that lies closest to Great Inagua). After Umbonis, the C. dimidiatum group is the most distinctive and peculiar of all Cerion phenotypes. Its forms bear several names in Cuba (C. dimidiatum, C. alberti, C. geophilus, C. disforme), but all include the flat-topped signature. These flat- topped Cerion form hybrid zones on Cuba with populations of other morphotypes (Galler & Gould, 1979). It seems clear, from morphological and genetic data presented below, that the modern flat-topped area effect within C. columna had its origin in the hybridization of this C. dimidiatum propagule with local Cerion columna-and that this area effect had its origin in a fortuitous phenomenon of history.

IV. MORPHOMETRICS OF THE AREA EFFECT (A) Material and methods We compared both the fossil propagule of C. dimidiatum (893) and five samples of the modern flat-topped area effect (central localities 892, 894, and 897 and western localities 898 and 899 at the zone of transition) with normal C. columna populations both west (852 and 853) and east (six samples from collections of the Department of Mollusks, Museum of Comparative Zoology) of the area effect. We also have comparable data for 59 other samples representing all major populations and phenotypes of Cerion on Great Inagua. We used the protocol of measurement followed in all our previous works (see Gould & Woodruff, 1978, 1986, 1987, for example)-20 shells per sample (when available), 18 direct measures and four derived ratios for each shell, including standard conchological features of size, weight, shape, ribbing, whorl sizes, protoconch, aperture, and umbilicus, with special emphasis on the determinants of Cerion’s complex, triphasic allometry (Gould, 1989). Easy identification of the protoconch (embryonic shell) providing a criterion for numbering whorls, and secretion of a terminal adult lip, permitting an assessment of variation among adults without the usual confounding effects of ontogeny, make Cerion an ideal biometrical subject. We have therefore been able to establish consistent patterns of covariance and to resolve the geometric determinants of differences in form (Gould, 1984a, b) . We performed factor analyses on the matrices of mean vectors for samples (14 for C. columna and the fossil propagule, 72 for all modern Inaguan samples). We also ran discriminant analyses on individual shells divided into groups of samples as described below (see Gould & Woodruff, 1978, 1986, 1987 for a description of programmes used).

(B) Distinctness of the area e$ct and its production by covariance A Q-mode factor analysis for the mean vectors of all 72 Inaguan samples shows the distinctness of the flat-topped area effect. The first five varimax axes each resolve more than one per cent of the total information and have clear biological interpretations. The first two dominate (at 92 per cent), and express the major contrast among the three Inaguan species-the larger size of C. columna 86 S. J. GOULD AND D. S. WOODRUFF and C. rubicundum us. the dwarf status of C. rehderi. The next three, each resolving 1.5 to 3.0 per cent of total information (see Gould & Woodruff, 1978, 1986 for a discussion of the potential biological significance of such small axes in analyses of mean vectors), express the most striking geographic variant within each of the three species-the north coastal ribby phenotype of C. rehderi, a fine-ribbed area effect within C. rubicundum in northern interior sections of the island, and the flat- topped area effect within C. columna (1.7 per cent of information). The dimension of the flat-topped area effect belongs to these samples alone, and not to C. columna in general. The five samples of the area effect exhibit all highest loadings on this axis, ranging from 0.094 (for one of the intermediate samples) to 0.372. All other C.coZumna samples load from -0.07 to 0.03. The factor scores for variables on this axis (Table 1) show the associations of covariance that have built the area effect by melding the distinctive features of C. dimidiatum into the C. columna stock. Widths of the embryonic shell, early whorls, and adult shell score positively, while shell length and number of worls are negative. We also note the pattern, pervasive in Cerion, that early widths correlate not with corresponding heights but with heights of later whorls-positive score for protoconch width and width at the fourth whorl (0.121 and 0.196), associated with negative score for protoconch height (-0.158) but followed by a continuous rise for heights of later whorls (-0.158 for protoconch, 0.098 for the fourth whorl, and 0.224 for fourth through sixth whorls). We have called this basic pattern in Cerion the ‘compensatory covariance’ (Gould & Woodruff, 1987), for it represents a feedback and negative interaction between the first two allometric phases (setting variation within Cerion’s beehive shape-Cerion means wax in Greek). Flat apices imply a subsequent intensification of height, while initially high apices engender a more modest increase later on and a relatively triangular appearance of the shell throughout growth. These opposing tendencies characterize the normal phenotypes of C. columna and C. dimidiatum-C. columna triangular and modestly expanding throughout, C. dimidiatum flat-topped and later parallel-sided with rapid growth in height. Since the area effect records an incursion of C. dimidiatum into C. columna, the flat-topped covariance of early widths with later heights dominates this axis. This expression of the compensatory covariance also explains the negative association of generally large widths with whorl number and height. Early whorls of the flat-topped area effect become unusually large as a result of their pronounced width (then maintained throughout growth), soon followed by increased whorl heights. Large whorls imply fewer final whorls for the trivial geometric reason that, when size is constrained (and flat-topped shells in the area effect are about the same general size as those of ordinary C. colurnna), large whorls imply fewer whorls to reach the same adult size. But, given Cerion’s allometry, this simple fact has further consequences for shape-particularly a relatively wide adult shell since Cerion adds height but no (or little) width during its later ontogeny, and restriction of whorl number limits the duration of this height-generating phase. This negative interaction of whorl size with whorl number and relative height-we call it the constraint covariance (Gould & Woodruff, 1987)-is the most pervasive pattern that we have identified in the growth of Cerion. It acts as a major determinant of shell form in all our studies (as reviewed in Gould, 1989). AREA EFFECTS AND CERZON 87 TABLE1. Factor scores for the axis expressing the area effect

1. Width of protoconch 0.121 2. Width at 4th whorl 0.196 3. Number of whorls -0.216 4. Density of ribs 0.1 16 5. Length -0.162 6. Width 0.084 7. Height of protoconch -0.158 8. Height at 4th whorl 0.098 9. Height from whorls 4 to 6 0.224 10. Width of umbilicus -0.026 11. Width of apertural lip -0.029 12. Thickness of apertural lip - 0.063 13. Height of aperture -0.022 14. Width of aperture -0.019 15. Rotation of aperture -0.069 16. Aperture to suture proximal -0.094 17. Aperture to suture distal -0.283 18. Weight -0.071 19. Shape ratio of aperture 0.525 20. Heightlwidth of entire shell -0.402 21. Width/height of protoconch 0.428 22. Width/height at fourth whorl 0.21 1

~ ~~

Direct measures of the aperture hardly contribute at all to this axis of the flat- topped area effect (measures 11-15), but the ratio measure of apertural inclination (19 of Table 1) scores strongly. Thus, the flat-topped area effect arises through the two major patterns of ontogenetic interaction in Cerion-the compensatory and constraint covariances of Gould & Woodruff, 1987-and represents the melding of the flat-topped and large whorled C. dimidiatum propagule into the C. columna stock. Scores for the three general shape ratios follow these expectations as well-relatively flat early whorls (0.428 and 0.21 1 for width/height of protoconch and fourth whorl) and a relatively wide final shell produced both by the general emphasis in width and by the limitation of whorl number described above ( - 0.402 for height/width of the entire shell). The distinctiveness of the flat-topped area effect is also evident in a univariate analysis of all samples for all Cerion taxa on the entire island. When each variable is ranked from 0 to 100 for its relative value across all 72 samples, the five samples of the area effect contain the extreme measure for ten of the 22 variables. Scoring maximally at 100 are measures of width (protoconch width in sample 894, fourth whorl and adult width in 897, width of the apertural lip in 898), ratios related to squatness (width/height of protoconch and fourth whorl in 897) and weight (897). Scoring minimally at 0 are early heights (protoconch and fourth whorl in 899) and adult heightlweight ratio (892). Note that all five samples of the area effect make contributions to these maxima and minima. By contrast, seven variables score 100 for an ordinary C. columna sample (either our 852 or 16007 of the Museum of Comparative Zoology): whorl number, length, height at whorl 4, height from the fourth to sixth whorl, apertural height, width and protrusion, and umbilical width. All these characters are either contrary to the thrust of the flat-topped area effect (large lengths and whorl 88 S. J. GOULD AND D. S. WOODRUFF TABLE2. Mean values of samples for flat-topped, fossil propagule standard C. colurnna area effect

Standard Area C. columna effect Fossil Character (N= 8) (X= 5) propagule

Width of protoconch 88.48 93.86 93.12 Width at 4th whorl 66.36 75.60 84.88 Number of whorls 8.789 8.273 7.792 . Length 33.72 29.91 28.15 Width 12.37 13.10 15.31 Height of protoconch 32.82 26.92 25.00 Height at 4th whorl 44.19 40.14 38.63 Height from whorls 4 to 6 51.16 50.03 61.30 Width of umbilicus .48.24 43.64 5 1.67 Height of aperture 90.25 83.39 83.50 Width of aperture 78.85 71.14 73.50 Rotation of aperture 30.38 26.3 1 29.00 Aperture to suture proximal 46.07 36.58 39.13 Aperture to suture distal 25.16 18.45 19.00 Shape ratio of aperture 1.868 2.092 2.122 Height/width of entire shell 2.727 2.292 1.829 Width/height of protoconch 2.742 3.572 3.640 Width/height at 4th whorl 1.509 1.908 2.252

Last four measures are ratios; whorl number is a count; length and width in mm; protoconch dimensions in micrometer units at high power (1 unit = 0.053 mm); all other measures in micrometer units at low power (I unit = 0.12 mm). numbers), or unrelated to it (apertural measures). Thus, the flat-topped area effect not only differs from ordinary C. columna but actually reverses some distinguishing features of growth in this taxon.

(C) Thefounding propagule as a morphogenetic source We did not include the fossil propagule, sample 893, in our full analysis because several measures (height, ribs and apertural lip) could not be taken due to problems of preservation. If we use the 18 available measures, and compare the fossil propagule with both flat-topped and normal samples of C. columna (Table 2), we find that ten of 18 variables form a monotonic series from normal C. columna through the area effect to the fossil propagule. All variables not fitting this pattern (with the exception of protoconch width and fourth to sixth whorl height) involve the aperture, which, as we have already argued (Table l), does not distinguish the area effect. Of the ten measures, the fossil propagule forms the minimal end of the series for whorl number, shell length, protoconch height, fourth whorl height, and heightlwidth ratio of the shell-and the maximal end for fourth whorl width, shell width, apertural shape ratio, and apical flatness (width/height ratio of the protoconch and fourth whorl). Note particularly how the propagule exaggerates the pattern of covariance discussed above as the ontogenetic cause of the flat-topped area effect: it is initially wider and flatter than all other samples, but height eventually catches up and surpasses all others as well, making general whorl size greater than for any C. columna. Large whorl size then feeds back, via the constraint covariance, to produce minimal whorl numbers and consequently minimal adult height. AREA EFFECTS AND CERION 89

TABLE 3. List of characters for which the propagule of the area effect is smaller or larger than average for typical C. colurnna

Larger than average Smaller than average

Width of protoconch Number of whorls Width at 4th whorl Length Width Height of protoconch Height from whorls 4 to 6 Height at 4th whorl Width of umbilicus Height of aperture Rotation of aperture Width of aperture Shape ratio of aperture Aperture to suture proximal Width/height at 4th whorl Aperture to suture distal Width/height of protoconch Height/width of entire shell

(The change in relative height is striking-and quite characteristic of C. dimidiatum, with its habit of growing rapidly down the axis of coiling after its abrupt shoulder and change of orientation to the second allometric phase. Height from apex to fourth whorl is minimal among the three categories for the fossil propagule, but height from fourth to sixth whorl is maximal.) If we compare the fossil propagule with all 13 samples of C. columna (standard and area effect), the fossils occupy an extreme for four measures-maximum for width at the fourth whorl, height from fourth to sixth whorl and apical flatness (width/height at the end of whorl four), minimum for height/width ratio of the adult shell. Table 3 contrasts the propagule with all others for characters greater and less than average for C. columna. As noted before, the propagule is smaller than an average C. columna for whorl number, adult shell height, early shell heights, and height/width rati-and larger for early widths, adult width, late whorl heights, umbilicus and early flatness. But we now also discern a coherent pattern for the apertural measures: the propagule is smaller in all four size measures (apertural height and width, and two measures of the whorl face just above the aperture), but larger in the two measures of change in apertural orientation at the third allometric phase (apertural rotation and shape ratio). Again, this pattern is characteristic of C. dimidiatum, reaching its extreme expression in the aberrant C. disforme with its highly constricted and contorted aperture (Clench & Aguayo, 1946; Gould, in press): initial whorls can be so flat that when compensatory growth in height occurs in the second allometric phase, the shell moves so rapidly down the axis of coiling that it actually constricts in width (as no other Cerion does), making the aperture and last few whorls smaller than those of earlier ontogeny. In summary, the C. dimidiatum shells of the fossil propagule exhibit three basic features of growth that distinguish them from the general pattern of C. columna. (1) A general emphasis on widths; (2) wide (but not high) early whorls followed by later increase in whorl height as well, leading by the constraint covariance to fewer total whorls and reduced relative height; and (3) a small but tilted aperture since whorl profiles do not continue to expand (and may even constrict slightly) at the end of growth. All these features are present, though muted somewhat, in shells of the flat-topped area effect us. standard C. colurnna. On these morphogenetic grounds, the origin of the area effect by hybridization seems clear. 90 S. J. GOULD AND D. S. WOODRUFF 3

I I I orea G. cohmna; intermediate effect I,, I I 1s- ' '

Figure 9. Factor loadings for mean vectors of all samples on a 3-axis Q-mode factor analysis. Typical C. columna samples cluster about axis 1, area effect samples and the fossil propagule about axis 2. Two samples of small shells have relatively high loadings on the third axis. The horizontal line towards the apex of the triangle depicts the univariate projection of each sample on the second axis alone-the main distinguisher of the area effect morphology. Note the complete separation of typical C.columna (both east and west of the area effect) in a tight cluster, and the intermediate status of the westernmost area effect samples 898 and 899.

As a final illustration of the morphogenetic affinity of the fossil C. dimidiatum propagule with area effect samples of C. columna, note how the propagule associates with the area effect, while both contrast with standard C. columna, in a factor analysis of all 14 samples. Figure 9 depicts factor loadings for mean vectors of all samples in a three-axis Q-mode solution (94.6 per cent of all information). The ordinary C. columna samples are all clustered tightly near the first axis; the area effect falls on axis 2, with the three central samples (892, 894 and 897) in an arc around the propagule (893), and the two intermediate samples more distant (898, 899). (The third axis, at ten per cent of information, pulls out an effect of small general size in two samples of minimal dimensions (899 in the area effect and MCZ 34504 in the eastern region of ordinary C.colunnu-size may vary widely within all regions and area effects of Cerion, see Fig. 4). Factor scores for the second axis show the basis of distinction for the area effect: strong early widths and flatness followed by gain in height, production of large whorls and subsequent constraint upon whorl number and adult height-all as previously discussed. Note highest scores (Table 4) for the three AREA EFFECTS AND CERION 91 TABLE4. Factor axes for the analysis of Fig. 9

Character Axis 1 Axis 2 Axis 3

1. Width of protoconch 0.057 0.337 -0.098 2. Width at 4th whorl 0.004 0.417 -0.090 3. Number of whorls 0.249 -0.072 0.540 4. Length 0.284 0.015 0.081 5. Width 0.088 0.320 -0.187 6. Height of protoconch 0.294 0.023 0.079 7. Height at 4th whorl 0.254 0.078 0.001 8. Height from whorls 4 to 6 0.162 0.255 -0.236 9. Width of umbilicus 0.290 0.111 -0.216 10. Height of aperture 0.260 0.076 -0.166 11. Width of aperture 0.271 0.072 -0.196 12. Rotation of aperture 0.244 0.085 -0.004 13. Aperture to suture proximal 0.354 -0.024 -0.043 14. Aperture to suture distal 0.37 1 -0.053 0.03 1 15. Shape ratio of aperture -0.123 0.380 0.278 16. Heightlwidth of entire shell 0.277 -0.068 0.500 17. Width/height of protoconch -0.128 0.434 0.359 18. Width/height at 4th whorl -0.1 15 0.402 0.126

measures of early and adult width (1, 2, and 5), for early flatness (17, 18), and for apertural tilt (15). Note also the continual increase of scores for successive heights until height from the fourth to sixth whorl achieves a high score as well (measure8). Scores for early heights, adult height and whorl number are all effectively zero. The first axis for ordinary C. columna shows the classic facies of a factor axis determined by general size Uolicoeur, 1963)-nearly all variables with low positive, and roughly equal, scores-all (in an interesting twist of this particular case) except the five measures of shell widths and initial flatness (1, 2, 5, 17, and 18). Thus, the first axis (standard C. columna) represents a growth to large size by the conventional route of adding height. (The small third axis records the pathway to small size of the two samples involved-proportionate reduction, producing an adult of the same number of whorls and shape, but of smaller size. Our programme normalizes each vector and therefore captures size in expressions of proportion within its own vector. Large loadings on the third axis are for whorl number (3) and ratios (15-18) that maintain average values across all 14 samples, but occupy more of their own vectors in these small-shelled samples because all linear measures have been reduced.)

(D) Discreteness of the morphological area efect Figure 9 underscores the two major arguments for the flat-topped area effect as a discrete and definable entity within C. colurnna. First, C. columna samples group together in a tight cluster widely separated from those of the area effect. Second, populations living west of the area effect (852 and 853) cluster indistinguishably with those from the east (the six Museum of Comparative Zoology samples), despite a geographic separation of up to 50 km, and despite a complete division of geographic range by the flat-topped area effect. In a discriminant analysis of all 13 C. columna samples, each treated as a 92 S. J. GOULD AND D. S. WOODRUFF separate group, 212 of 237 specimens (89.5 per cent) fell closest to their own centroid. But not a single specimen from any area effect sample stood closer to any centroid for an ordinary C. columna sample. The first discriminant axis resolves 45 per cent of the variation among centroids and makes a clear and primary separation between the area effect and ordinary C. columna (with the intermediates, 898 and 899, in between but closer to the area effect). Figure 10 shows the same two phenomena of discreteness-clear phenotypic gap between area effect and ordinary C. columna, and grouping together of C. columna samples living both east and west of the area effect. Thus, in both factor and discriminant analyses (Fig. 9), the area effect appears as a well-defined and delineated anomalous phenotype within the range of a stable taxon, not just as one hump in a complex and continuous gradient of morphology.

V. GENETICS AND THE AREA EFFECT Our study of morphological variation in Cerion on Great Inagua has been paralleled by a study of geographic variation in genetic features. We have surveyed allozymic variation in most of the same individuals studied morphometrically; patterns of genetic variation have been established for more than 100 samples representing every known taxon and accessible habitat. The results of these comprehensive surveys will be published elsewhere in the context of a monographic revision of the Inaguan Cerion faunas. Here, we simply report that the morphologically defined area effect is highly coincident with a genetic area effect. Cerion species, like those of many birds, are very similar to one another allozymically. The semi-species on an island or island bank form a syngameon whose members are characterized by parapatric distributions delimited from adjacent taxa by narrow hybrid zones. Not surprisingly, the interspecific genetic distances (Nei, 1978) are small, typically 0=0.05-0.10 (Gould & Woodruff, 1978, 1986, 1987). Nevertheless, genetic patterns have been extremely useful in reconstructing the evolution of this taxonomically difficult group. Although genetic homogeneity may be the norm in these species, genetic heterogeneity or anomaly has been highly informative. Three types of allozymic inhomogeneities have been recognized. First, in Cerion, as in other organisms, we detect rare alleles occasionally in an unpredictable fashion. Such localized alleles are truly uncommon and, unfortunately, not observed often enough to be employed in reconstructing dispersal patterns and other historical aspects of gene flow (Slatkin, 1987). Second, the hybrid zones between semi-species are typically areas of genetic anomaly characterized by the presence of unexpected alleles at 5-20% of the loci surveyed. These unique alleles, termed hybrizymes, are usually associated with polymorphic loci sharing the same variability in both parental species (Woodruff, 1989). These two kinds of genetic anomalies stand in contrast to the phenomenon of area effects, representing anomalies of a third type: those left over after episodes of colonization and introgressive hybridization. In the two cases reported previously (Gould & Woodruff, 1986; Woodruff & Gould, 1987), we found localized areas of elevated genetic diversity within an otherwise genetically homogeneous array of conspecific populations. The genetic area effect covered an area many times the size of a single colony or neighbourhood and was not associated geographically with any conspicuous microhabitat patch. AREA EFFECTS AND CERION 93 A AA I I EE WEEW E 6 1 I1 I I -

2 *852 m 0853 c"0 X a ,892 -2 X894

-4

-6 I I I -5 -3 -I I 3 5 AXIS I Figure 10. Centroids for area effect (crosses) and typical (dots) C. columna samples plotted against first and third axes of a discriminant analysis. The top horizontal line shows projections on the first axis alone. A = central area effect; I =intermediates of western area effect; E = typical C. columna east of the area effect; W = typical C. columna west of the area effect. Note separation of all area effect from all typical centroids and tight clustering (without distinction) of typical centroids both east and west of the area effect.

We have found, once again, a similar situation on the north coast of Great Inagua-right in the region of the morphological area effect. Using starch gel electrophoresis we surveyed allozymic variation in 171 adults in 12 samples representing 7 geographic sites within 2.5 km of locality 892. Our techniques are described elsewhere (Woodruff, 1975; Gould & Woodruff, 1986). Individual snails were scored for variation at 20 genetically interpretable allozyme loci. Twelve loci were monomorphic in this area: Aat-2, Crp, Es-5, ES-6, Glydh, Idh-1, Idh-2, Lap-1, Mdh-1, Mdh-2, Sod-1, Sod-2. Eight loci were polymorphic in at least one population: Aatk-1, Es-1, Es-2, Gpi, Lakp-2, Ldh, GPgd, Pgm-2. Of this second group, three loci exhibited alleles restricted to the region of the morphological area effect: Es-p Gpi6 and Ldh6. These three alleles have not been detected among more than 1500 snails studied from elsewhere on Great I nagua. The distribution and frequency of the three alleles forming the genetic, area effect is described in Table 5 together with summary data on genetic variation in all 12 samples. The genetic anomaly is restricted to localities 894 (both samples) and 892 (only in the larger sample). These three samples are more variable than 94 S. J. GOULD AND D. S. WOODRUFF TABLE5. The genetic area effect*

Frequency of alleles not detected elsewhere

Taxon Sample NAP A Es-T Gp? Ldh'

C. columna 894a 30 1.4 0.35 0.16 0.05 0.02 0.05 894b 24 1.4 0.35 0.16 0.06 0.02 0.08 892a 27 1.4 0.30 0.13 - 0.04 0.02 892b 6 1.3 0.25 0.15 _. ~ ~ 897 9 1.2 0.20 0.12 - ~ ~ 898 9 1.3 0.25 0.14 _. ~ ~ 899 10 1.3 0.20 0.12 - C. rehderi 899 23 1.2 0.20 0.11 90 1 10 1.1 0.15 0.11 902 15 1.2 0.20 0.12 C. rubicundurn 90 1 4 1.2 0.20 0.13 902 4 1.1 0.10 0.10

*The sample localities are shown in Fig. 6; N, sample size; A, me_an no. of alleles per locus; P, proportion of 20 loci studied that are polymorphic; H, mean individual heterozygosity by direct count. the others. The novel alleles extend at least 700 m along the coast, but were not detected in conspecific samples 500 m inland (897) or 2.5 km further west (898 and 899). As the alleles were detected at frequencies of only 0.02-0.08, it is unclear whether our failure to detect them in the surrounding samples is due to smaller sizes of these samples, or to restricted geographic distribution of the alleles. There is no evidence that these alleles ever introgressed into C. rehderi or C. rubicundum (899, 901, 902) 0.5-1.5 km south of the coast. In the case of the two previously described genetic area effects, the source of the anomalous alleles was known. We used historical records to trace the geneology of the Bahia Honda (Florida) Cerion back to their native South Andros (Bahamas) 50 years earlier (Woodruff & Gould, 1987). On New Providence, we were able to show that an area of elevated variability within the range of C. gubernatorium could be attributed to the presence of genes from C. agassizi (Gould & Woodruff, 1986). Cerion agussizi occurs on nearby islands today but the colony that used to inhabit New Providence has all but disappeared as a result of introgressive hybridization with C. gubernatorium. Only its phantom remains. In contrast, the origin of the genetic area effect on Great Inagua cannot be resolved at this time, since we have no data on the genetics of the probable ancestral population, C. dimidiutum, in Cuba. Until such data are available we cannot be certain about the source of Es-r' and the other unexpected alleles. We hypothesize that these alleles were introduced from Cuba by hurricane transport of C. dimidiatum-like snails. Subsequent introgression between the widespread C. columna and the small and geographically restricted colony of introduced snails has left the genetic phantoms reported here. The precise geographic co- occurrence of the unique genetic and morphological anomalies, combined with strong morphometric evidence linking the modern area effect with a fossil AREA EFFECTS AND CERION 95 propagule of C. dimidiatum type, indicates that the genetic and morphological area effects have a common historical explanation. The duration of such genetic phantoms depends on many factors, including the selection coefficients of the various genotypes, the effective population size and gene flow parameters of the interacting species, and the initial frequency of each allele in the colonists. A consideration of the known history of the Bahia Honda case, for example, suggested that these phantoms may ‘disappear’ within 500 years (Woodruff & Gould, 1987). Our island-wide survey of genetic variation on Great Inagua has revealed several other genetic area effects. One on the east coast is intriguingly similar to the effects described above; in C. rubicuncum from three localities near Dog Head Point, we found two alleles (at two loci) that have not been encountered elsewhere in the 120 km linear range of that species. Subfossil Cerion in this area (C. excelsior, see Gould, 1984b) is very different from the present-day inhabitants. Again, the current distribution of the phantom alleles may permit us to reconstruct the local history of the Cerion syngameon in this area as well. As noted in our earlier review (Woodruff & Gould, 1986), history and immediate context, chance and adaptation, have been major determinants in this group’s evolution. The geographic concordance of morphological and genetic area effects in Cerion points to a promising way for the development and testing of historical hypotheses.

VI. CONCLUSION: ON THE POWER OF HISTORY With this consilience of paleontology, morphology, biogeography, and genetics, we believe that we have established a nearly conclusive case for an area effect initiated by happenstances of history rather than selective forces of current environments. The flat-topped area effect within C. columna at Rocky Harbor arose by introgression from a propagule of the C. dimidiatum stock, and not as a consequence of advantages for squat shells in this short stretch along the coastline of northern Great Inagua. Although evolution is, intrinsically, a science of history, our profession has generally steered away from explanations rooted in contingencies of past events, and strongly preferred non-historical approaches based upon predictable forms of ‘perfection’ or ‘suitability’-the move to ‘equilibrium thinking’ in ecology, to optimal foraging theory in social behaviour, or to panselectionist accounts of morphology. The reasons for this curious neglect of history (by a subject so wedded to connectivity in time) are many-some bad, some understandable. Among bad reasons, we may cite the thrall imposed by conventional status orderings that rank physics at the top and natural history too near the bottom of a linear array stretching to supposedly soft and squishy disciplines like sociology and psychology on the bottom. Since narratives based on unique contingencies seem furthest removed from the ‘high status’ activities of quantification and experimentation, they qualify as approaches to be avoided, even though nature owes its shape to such complex histories. All scientists should reject this false and stultifying view of disciplinary interactions. Among good reasons, we must admit that the need for extensive knowledge of particular contingencies does place many products of history into the realm of the scientifically intractable, given the 96 S. J. GOULD AND D. S. WOODRUFF poor survival and preservation of historical information. Still, no one ever said that nature would be simple, and proper paths cannot be avoided because they impose burdens of inconvenience. In response to this dilemma of history as so essential yet so elusive, we have written a two-part paper with a single concern-to document the importance of historical contingency in the explanation of area effects. In the first part, we present a review, in this context, of the original definition and subsequent debate over area effects for the ‘type’ example of Cepaea. We argue that historical contingencies of bottlenecks and invasions into formerly unsuitable habitats may explain the classic area effects better than selectionist interpretations originally proposed. We also contend that the focal issue of historically contingent us. currently optimal can provide a much more fruitful basis for discussion than the conventional dichotomy of adaptive us. random. In the second part, we report our discovery of a historically contingent area effect within Cerion columna on Great Inagua, Bahamas. We regard this example as particularly favourable to our general aim for two reasons. First, it presents a historical explanation of a type (immigration and introgression) different from Cameron’s for Cepaea (bottlenecks and creation of favourable habitat). Historical explanation is a broad category, not a particular scenario. Second, through good fortune of unusual density in preserved information, we have been able to assemble all the key empirical pieces to validate a historical explanation-a circumstance unfortunately rare, given the general poverty of preserved evidence. We have found fossils of the propagule, cemented into carbonate soil crusts in the region of the current area effect. We have linked the morphological peculiarities of the area effect to the phenotypic oddities of the propagule by criteria of multivariate patterns in clustering of correlations, not only in subjective appearance. Moreover, we have found unique alleles within populations of the area effect-genetic markers detected nowhere else within Cerion columna, or in any other taxon anywhere else on Inagua. Such unexpected alleles represent genes originally introduced with C. dimidiatum or are hybrizymes produced by interspecific hybridization (Woodruff, 1989). History may be as elusive as a thief in the night, but the only honourable response is diligence and ever-improved forensics. The subject is as important to our science as the contingent history of the man who used that simile to describe his impact (1 Thessalonians 5:2) has been to the earthly fate of Homo sapiens.

ACKNOWLEDGEMENTS The greater part of Inagua has no roads or trails. To Jimmy and the late Sammy Nixon, the only men on earth who know the interior of this island, we owe our deepest and absolutely indispensable thanks. They led us in the field and showed us the only overland route to Rocky Harbor, where we found the flat-topped area effect. For measurement of specimens, Gould thanks Kurt Wise, and for computer programming and organization of data Ned Young and David Backus. Support for field, laboratory, and morphometric work was provided by National Science Foundation Grant Nos. BSR 8607045 and BSR 8807241.

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