A Remarkably Diverse Group of West Indian Land Snails1'2

MALACOLOGIA, 1978, 17(2): 223-239

EVOLUTION AND ADAPTIVE RADIATION OF CEBION: A REMARKABLY DIVERSE GROUP OF WEST INDIAN LAND SNAILS1'2

David S. Woodruff

Department of Biological Sciences, Purdue University, West Lafayette, Indiana 47907, U.S.A.

ABSTRACT

The pulmonates of the genus Cerion are remarkable for the extreme variability of their shells. The vast array of shell types present in Cuba and the Bahamas, coupled with past typological taxonomic practices, has resulted in the naming of over 600 "species." The complex patterns of geographic variation are so confusing that several workers have despaired of the possibility of ever applying the biological species concept to this group. The allegedly haphazard distribution of fossil and living shell types has been attributed to the vagaries of

hurricane dispersal. Stephen Jay Gould, of Harvard University, and I have been collaborating on a holistic study of the geographic variation, ecology, and evolution of these remarkable snails. We have begun to make sense of this extraordinary situation by detailed mapping of geographic variation in the field and by laboratory studies of multivariate morphometries and biochemical genetics. So far we have found that the 200 "species" of the northern Bahamas reduce to a single pair of contrasting morphotypes: phenetic and genetic variation is continuous rather than capricious. Furthermore, while hurricanes may have played a role in establishing some distribution patterns, their importance appears to have been overestimated. In the northern Bahamas, we can discern an overall biogeographic pattern that appears to have evolved in situ during the late Cenozoic. As a result of these studies and others involving Cerion from elsewhere in the Bahamas, Cuba, Hispaniola, Puerto Rico, the Dutch Leeward Islands, and the Florida Keys, we anticipate a downward revision of close to two orders of magnitude in the number of valid species. Despite the enormous taxonomic literature on Cerion, we know remarkably little about its natural history or the adaptive significance of the variation in shell morphology. It was widely held that the snails are obligate halophiles, that they are restricted to a zone close to the shore, and that their abundaoce (up to 212 per square meter) stems from a lack of prédation. Field observation over the last few years has shown that these beliefs are unfounded. Long-term ecological studies in the northern Bahamas have been initiated in an attempt to generate some basic information on population size, dispersion, dispersal, growth rates, prédation, and mortality. The activities of over 1,500 individually marked snails have been followed periodically since November, 1973. Laboratory studies on the mechanical strength and thermal properties of the different shell types are also being conducted to try to establish the adaptive significance of the observed morphological variation. The results of these studies will be presented, and, in addition, attention will be drawn to a number of other outstanding problems (including Cerion'% ability to estivate for protracted periods) presented by these animals. In a broader context, Cerion will be shown to display one of nature's most impressive displays of morphological variety. While this diversity has been acquired without widespread speciation or extensive genetic differentiation, the group provides prime material for studies of the genesis and maintenance of morphological complexity.

INTRODUCTION gradations, that naturalists do not like to rank them as dis- 'Those forms which possess in tinct species, are in several re- some considerable degree the spects the most important to character of species, but which us." (Darwin, 1859: 47). are so closely similar to some other forms, or are so closely "A genus in which many such linked to them by intermediate situations seem to occur is the

^This review is No. 10 in a series on The Natural History of Cerion. It is respectfully dedicated to William J. Clench and Ruth D. Turner who first introduced the author to Cerion. ^This research was supported, in part, by grants from the U.S. National Science Foundation to S. J. Gould and the author.

(223) 224 WOODRUFF

snail genus Cerion, considered NATURAL HISTORY "the most difficult genus of pulmonate mollusks to classify" Snails of the genus Cerion Röding are (W. J. Clench, in litt.)" (Mayr diverse and conspicuous members of the & Rosen, 1956: 1). West Indian land snail fauna. They are found in the Florida Keys, Bahamas, Cuba, The West Indian pulmonate Cerion is Cayman Islands, Hispaniola, Puerto Rico, celebrated in the evolutionary literature for Virgin Islands and the Dutch Leeward its phenetic diversity. Intrapopulation varia- Islands. They are generally restricted to tion is rarely extraordinary in extent, but coastal areas where they are typically shells of each local population develop dis- found along a narrow strip of open vegeta- tinctive features, and an astonishing range tion within 100 m of the shore. Cerions are of forms is found in certain parts of Cuba abundant in their preferred habitat, often and the southern Bahamas. Differences in reaching densities of 10 adults/m^ and at- shell size, shape, sculpture and coloration taining colony sizes of lO'' individuals. have been used to characterize almost 600 While the vast majority of cerions are typi- species and the evolutionary importance of cally found hanging in the plants, to which these remarkable animals has been buried they seal themselves with a thin epiphragm, under an all but impenetrable taxonomic a few species live in the leaf litter and thicket. This is to be regretted as recent sand. Very little is known about their studies show Cerion to be prime material ecology and behavior beyond the casual for the examination of a number of impor- observation that they spend the greater tant biological problems including the rela- portion of their adult lives in a state of tionship between growth and form, the estivation. Inactive during the day, they are maintenance of genetic and phenetic varia- thought to emerge and feed at night, when tion, the genodynamics of hybrid zones these areas are actively tenanted by mos- and the processes of geographic speciation, quitos and sandflies, and malacologists have and the evolutionary biogeography of spe- retired from the scene. cies distributions. The most remarkable thing about Cerion

In this paper I review the results of a is, of course, the great variation in shell decade's work on Cerion by Stephen Jay morphology (Figs. 1-13). It has become Gould and myself. Gould, a paleontologist apparent that nearly every local population and biometrist, was attracted by Cerion's has a diagnostic size, shape, sculpture and basic diversity, by its good fossil record in color. Most of the published work on the Pleistocene dunes, and by the pro- Cerion is devoted to partitioning this varia- pensity of most individuals to display their tion among nearly 600 species. (Mercifully, entire ontogeny in an accessible shell. In Clench (1957) has prepared an authorita- contrast, I initially approached Cerion be- tive catalogue of this vast taxonomic litera- cause of its abundance and distribution ture.) Plotting the locality records for these pattern, characteristics that made it suitable taxa produces a crazy-quilt distribution pat- for an experimental study of the relation- tern for many species (see Gould & Wood- ship between the ecological genetics of ruff, 1978: fig. 1). There is marked geo- natural populations and distribution. Our graphic variation with adjacent populations collaboration quickly transcended these being radically different from one another. personal interests and many of the studies Several species found on Long Island in the reported below should be attributed to Bahamas are shown in Figs. 7-13; steven- both workers rather than the author alone. soni and C. fernandina occur within 200 m While we have learned a great deal about of one another. Elsewhere in the Bahamas Cerion only a small fraction of our findings and Cuba different species replace one an- have yet been reported. Accordingly, I will other in irregular fashion along the coasts. describe some of our on-going projects, This unusual pattern of shell-type both to report on our progress (or lack of (morphotype) distribution is probably real; it) and to indicate problems to which other Cerion is an extremely well-collected group. investigators may hopefully be attracted. The record does, however, embody two This paper, then, constitutes no more than erroneous factors that must be noted at the a prolegomenon to the evolution and adap- outset. First, I can substantiate no case of tive radiation of these remarkable animals. sympatry between any of the species re- NATURAL HISTORY OF CEBION 225

FIGS. 1-13. The phenetic diversity of Cerion displayed by selecting average specimens of taxa discussed in the text. The bar represents 1 cm. 1, C. uva. Curaçao; 2, . bendalli. Little Abaco, Bahamas; 3, . abacoense. Great Abaco, Bahamas; 4, C. glans. New Providence, Bahamas; 5, incanum. Big Pine Key, Florida; 6, pauli. Great Exuma, Bahamas. Bottom row, all from Long Island, Bahamas; 7, caerulescens 8, eximeum; 9, nudum; 10, sp. indet. (? dwarf caerulescens); 11, C. malonei; 12, C. (Umbonis) Stevenson/'; 13, . fernandina. ported by earlier workers to coexist. Mayr's distinct populations come together in na-

(1963: 398) report for eastern Cuba is ture they appear to be able to interbreed. compromised by the presence of clear in- Thus, while the apparently haphazard dis- termediates in his sample. Other alleged tribution of morphotypes in some areas is cases arise from the custom of some earlier real, the pattern is the result of a mosaic of conchologists to artificially sort their sam- contiguously distributed morphotypes ples into dissimilar types without regard for rather than the coexistence of different the natural intrapopulational variation. Still species in different combinations. Until the another source of confusion comes when a taxonomic status of these morphotypes is sample contains both living and dead speci- reestablished we can say almost nothing mens. Crabs and various forces of nature about the specific diversity of different carry dead shells vast distances and result islands or the genus as a whole. in heterogeneous populations of shells. Er- The so-called species of Cerion are char- rors of this type must be borne in mind acterized exclusively on the basis of shell when examining the literature and older characters. Four subgenera and 15 species museum collections. The second type of groups have been proposed (Pilsbry, error in the record arises, in part, from the 1901-1902) on the basis of features which typological systematics practiced by the may or may not have phylogenetic signifi- early Cerion specialists. Dissimilar forms cance. Two subgenera contain single spe- were named as separate species without any cies: Eostroptiia, for anodonta from regard for their interactions in the field. Oligocène deposits in Florida, and Cerion,

The truth of the matter is that wherever for the type-species uva from Curaçao. 226 WOOD RUFF The name cerion, derived from the Greek various morphotypes (Gould et a!., 1974; word for a honey-comb, alludes to the Woodruff, 1975b; Gould & Woodruff, resemblance of C. uva to an old-fashioned 1978; Woodruff & Gould, in prep.). An bee-hive (Fig. 1). The vast majority of analysis of the observed genotype fre- living cerions are referred to the subgenera quencies in each sample revealed that Strophiops and Diacerion depending on the Cerion, a facultative hermaphrodite, is ap- form of the axial and parietal teeth in the parently outbreeding. Cerion populations aperture of the shell. However, as Pilsbry (large and small, but with one notable himself noted (1901-1902: 179), the dis- exception reported below) studied to date tinction between these groups breaks down have moderate amounts of genetic varia- in some forms. The remaining subgenus, bility: mean number of alleles per locus,

Umbonis, is the only species group to have 1.65-1.70; frequency of loci polymorphic received any recent attention (Clench & per population, 0.15-0.30; and frequency Aguayo, 1952). The shells of this group are of heterozygous loci per individual, quite characteristic in their shape, in having 0.054-0.128. The systematic and evolu- spiral sculpture of numerous incised lines, tionary significance of these findings will and in agglutinating small sand grains to be discussed in the second half of this review. the outside of the shell. The group includes As noted previously there were virtually Stevenson! from the northeast coast of no quantitative data available on the Long Island (Fig. 12) and 13 other species ecology of Cerion. Accordingly, in Novem- from the Bahamas and Cuba. A dwarf ber, 1973, I established two study sites on form, turnerae, occurs on Great I nagua Great Abaco Island in the northern and reaches a length of 15 mm (see Gould Bahamas. The sites were chosen to char- et al., 1974: fig. 1). acterize high density populations of two The anatomy of several species of morphotypes found throughout the Cerion has been studied; Richter (1926) Bahamas. One area (Rocky Point) is in- and Jaenicke (1933) did some careful work habited by C. bendalli which has a thin on uva from Curaçao and . g/ans from shell which is smooth or finely ribbed and New Providence in the Bahamas. Unfor- mottled with brown and black (Fig. 2). tunately, it is difficult to assess the alleged The other area (Shipwreck) is inhabited by differences in the digestive, nervous and abacoense, a species with a heavy white reproductive systems until comparable shell with prominent ribs (Fig. 3). All snails studies have been made to establish the at these study sites have been individually extent of intraspecific variation due to the marked, in situ, a process which has a very age, behavior and physiological state of the slight effect on dispersal but no discernible snail. Dissections of some other species effect on growth rates and survival. The (including incanum from Florida) are populations have been censused repeatedly figured by Bartsch (1920) and Pilsbry over a four year period and data are now (1946), but there are numerous points of in hand for over 1600 snails. As the data disagreement and the work will have to be analyses are continuing much of what is repeated. reported here should be regarded as pre- Burch & Kim (1962) have described the liminary. karyotype of incanum: the diploid num- At the start of these studies snail den- ber is 54. Twenty-seven pairs of chromo- sity at Rocky Point averaged 13 adults per somes have also been found recently in C. m^ (range, 0-79). Similar densities occurred fernandina by Michael Goldman in my at Shipwreck. Typically over 90% of the laboratory. adults at both sites are found off the Studies of genetic variation of Cerion ground attached to stems and leaves. They have added a new dimension to our under- show a strong preference for certain plant standing of the evolution and adaptive radi- species like the lily, Hymenocal/is declinata. ation of these snails (Woodruff, 1975a). The juveniles (typically 10-20% of the pop- Using electrophoretic techniques (Wood- ulation) are found on the soil surface be-

ruff, 1975b) I have examined variation in neath the shallow leaf litter or at the base more than 20 enzyme systems in several of clumps of grass or bushes. Mark-release- thousand snails from various parts of their multiple recapture studies indicate that the

is range. I have identified more than 30 neighborhood area less than 100 m^ and allozymes or structural gene products and that the effective population size (N of begun to study their distribution in the Wright, 1946) is approximately 1000 snails. NATURAL HISTO RY OF CER ION 227 Gérions appear to spend the greater part less continuously in the open vegetation of their adult lives attached to the vegeta- that parallels the beach. The variance of tion in a state of estivation. They are dispersal along an axis parallel with the typically encountered sealed (aperture up) beach follows a pattern that we might by a thin epiphragm to the stems and expect for snails making random move- branches of low bushes or the leaves of ments on a large habitat patch. (The vari- monocots. How long they rennain in estiva- ance for the first 12 month period is tion in nature is unknown and probably greater than that for either component 6 varies between individuals in response to month period, although it is not the sum spatial and temporal changes in the micro- of the two, as would be expected for environment. In the laboratory I find that completely random movements.) The move- the larger species will estivate for over 24 ment of snails with respect to an axis at months if undisturbed. In the field, adults right angles to the shore shows a com- are found moving about at night and dur- pletely different pattern: the 1 year vari- ing the day following rain. They have been ance is actually less than that for either 6 observed both moving among the leaves of month period. This indicates that the snails plants and on the ground surface. Diet is perceive the vegetation change along the still poorly defined. Contrary to Bartsch's beach front (and further inland) and move (1920: 6) statement that adults feed on back into the habitat patch. fungal mycelia, other investigators have The statistical interpretation of these found vascular plant remains in the feces data is difficult because several of the (Weston, in Mayr & Rosen, 1956; and June parameters are not normally distributed. Chatfield, National Museum of Wales, in However, if we make some simplifying (and litt). While cerions do not damage the reasonable) assumptions, it is possible to plants with which they are associated they estimate some very important demographic may graze on decaying plant material. parameters. If one assumes that generation

Cerions at Rocky Point and Shipwreck time at Rocky Point is 5 years (see below) are highly sedentary. Some snails have re- then I estimate the mean distance displaced mained on the same plant for 2-3 years. per generation to be 200 cm (range With the assistance of Annette Adams in 100-400 cm). The evolutionarily important my laboratory I have devoted considerable gene flow distance may then be estimated attention to dispersal behavior as it is es- as the product of the mean distance trav- sential that we be able to estimate the elled in a generation and the square root of magnitude of gene flow if we are ever to the probability of leaving a deme or neigh- understand the microevolution of these ani- borhood (May et al., 1975). For a high mals. As expected, adult dispersal patterns density population of bendalli at Rocky are leptokurtic. In the first six months Point my preliminary estimate for this

(winter) of my study at Rocky Point the parameter is 2.8 m. The significance of this mean detected displacement was 107.7 cm low value will be discussed later in the (range, 0-1202 cm, N - 109). In the follow- context of the maintenance of dines and ing six-month period (summer) the mean narrow hybrid zones. displacement was 215.7 cm (range Given its moderate size, Cerion's abun- = 0-2200 cm, N 221). In each census pe- dance is remarkable; in its favored habitats riod a significant number of adults it is far commoner than He/ix, Cepaea and (11-16%) were recaptured on the plant other land snails that have been subjected where they were first encountered. Using to ecological scrutiny. In our field work we Batschelet's (unpublished) ellipse of inertia have come to designate Cerion as being technique to compare dispersal in succes- locally rare, uncommon, common and very sive census periods I concluded that the common at average densities of 0.1, 1.0, 10 adults move more during the wetter sum- and 100 adults per m^, respectively. It is mer months than during the winter. Dis- not unusual to find aggregations of living persal is not random with respect to direc- snails numbering between 100 and 150 tion; it is clearly constrained by the size individuals on a single bush. In this respect and shape of the habitat patch and by the it is not unlike the Mediterranean land distribution of plants within the patch. At snail, Theba pisana. Density of dead shells Rocky Point, for example, the study site can be even higher (up to 245 per m^), but lies about 30 m inland from the high water this is misleading indicator of natural den- mark and the snails are distributed more or sity and dispersion. The shells accumulate 228 WOOD RUFF on the ground surface and are resistant to also eat Cerion; one side of the shell is deconnposition. In sonne areas of the characteristically sheared off leaving both Bahamas these dead shells carpet the the lip and protoconch intact. Still another ground surface at densities ten times that predator, possibly a bird, is implicated by of the living snails. In their favored habitat the discovery in the pine forest of Grand cerions are about ten times as abundant as Bahama Island of an "anvil" surrounded by the next most common land snail; usually a irregularly broken shell fragments. Finally, member of the genus Hemitrochus I note that cerions interact with still an- (Cepolis). other organism which breaks a small round Cerion's abundance has traditionally hole in the shell. It is not yet known been attributed to a lack of prédation; fires whether the hole is made from within or and hurricanes being generally recognized without; it is subsequently repaired. as the main factors determining a colony's As these anecdotes indicate, we still success. The common occurrence of areas know very little about the ecology and with vast numbers of dead snails but very behavior of Cerion. The deficiencies are few living snails is cited as evidence for the particularly apparent in the area of repro- significant role of natural disasters. Un- ductive behavior where we badly need to doubtedly, natural and man-made brush establish whether there are specific behav- fires have a devastating effect on Cerion. ioral traits that could serve as pre-mating The impact of a hurricane has yet to be isolating mechanisms between the various formally established (fortunately my study morphotypes. A knowledge of Cerion's sites have yet to be perturbed in this mating system and reproductive strategies is manner). Again, the traditional wisdom is also required if we are to understand the that the colony is destroyed and a few adaptive radiation of these snails. Unfor- fortunate, fertilized individuals survive to tunately, repeated attempts to induce colonize new habitats into which they are courtship and mating in the laboratory introduced by the wind or water. Cerion's have failed so we are still limited to some ability to survive immersion in sea water opportunistically gathered observations. I has been described by Bartsch (1912) and have seen mating once in the field, follow- Mayr & Rosen (1956). One case might be ing an afternoon cloudburst in June on cited as evidence that hurricanes may erad- New Providence. Copulation is protracted, icate some colonies: C. chrysaloides disap- taking at least 2 hours, and is not recipro- peared from its former habitats on the cal. Pairs of snails lie on the ground surface southwestern coast of Grand Bahama Island with their apertures adpressed. Several mat- following a "direct hit" in the 1930's ing pairs were returned to the laboratory (Clench, 1938; Gould & Woodruff, 1978). where additional matings between some of On the other hand, the continued existence these pairs were observed. About 3 weeks of Cerion on innumerable low lying cays in after the original matings some snails began the Bahamas suggests that some individuals to excavate small egg-chambers at a depth survive and repopulate these environments. of 2-4 cm in moist sand. Batches of 4-7 High recapture rates of adults at Rocky eggs were layed in some of these chambers Point and Shipwreck (80% after 6 months (details will be presented elsewhere: Wood- and 40% after 48 months) indicate that ruff, in preparation). The egg capsule is adult mortality is low. Observations there, initially colorless but gradually turns and elsewhere, indicate that cerions do in opaque and white, suggesting a calcareous fact experience significant losses to a num- matrix. (Capsular fragments have been sent ber of predators. Land crabs (Gecarcinus to Alex Tompa, University of Michigan, for lateralis at Rocky Point) take a number of analysis.) Juveniles began to hatch about snails on the ground and may provide part 20 days later and emerged from the sand of the selective force that causes the snails about a week after that. Studies of the to estivate just above ground level. Typi- growth and development of these snails cally, these crabs will carry the snail back (N = 212) are being conducted by Sarah to the entrance of their burrow before Burgess in my laboratory. Not only will breaking the shell into small pieces and these observations provide us with informa- removing the animal. Small piles of shell tion about growth but, as we have the fragments, often with the lip intact, may parents of each group of juveniles, we hope be found around the edge of the sand pile to learn something about the heritability of surrounding an occupied crab hole. Rats shell traits too. NATURAL HISTO RY OF CERION 229 Additional information about growth biminiense and pillsburyi. Mayr & Rosen rates is coming from studies of marked stress, however, that even though super- juveniles at Rocky Point and Shipwreck. ficially each morphotype appears to be a Unfortunately, the data on juveniles are separate species, each is allopatric, and not as extensive as that for adults as the adjacent colonies show signs of gene ex- former experience quite high mortality change. rates. Juveniles grow very erratically: in Mayr & Rosen argued that these facts one 6 month period a snail might lay down were best explained by assuming that the a single rib while in the next 6 month pattern was controlled by two antagonistic

period, perhaps two whorls. Although I tendencies: a high degree of sedentariness suspect reproduction and hatching occur and infrequent long-distance dispersal by during the summer the subsequent growth hurricanes. The checkerboard pattern of

pattern is not strongly seasonal. My pre- morphotype distribution arises as a result

liminary conclusion is that individuals at of multiple colonizations of each island, these localities are typically 3 years old extensive hybridization of types secondarily when they secrete the lip characteristic of brought into contact with one another, and the adult shell. This conclusion is sup- a steady extermination of colonies as a ported by laboratory growth experiments result of fires and hurricanes. They inter- conducted by Ida Thompson (Princeton preted the readiness with which the three University). To calculate the generation morphotypes hybridized, in spite of pro- time (estimated above to be 5 years) we nounced morphological differentiation, as

need to know the age of sexual maturity. evidence that reproductive isolation is not On this subject we have no information. easily acquired in this genus. In contrast, However, as some snails live at least a they argued that shell characters are highly

decade after laying down the adult lip I plastic and evolve rapidly during the early have conservatively assumed that they are stages of colonization, adapting the snails reproducing successfully in their second to their new environment. They wrote "In

summer of adult life. I tentatively conclude view of the fact that these snails are her-

that cerions are outcrossing, iteroparous maphrodites it is possible and probable that

hermaphrodites with generation times of many if not most colonies are founded by 4-5 years and a longevity of perhaps twice a single fertilized adult. Two factors tend that duration. to promote rapid divergence in such colonies. Comparatively high inbreeding among the early generations derived from the founder individual exposes homozygous RECENT STUDIES WHICH FOCUS ON genotypes more often to selection than in THE SYSTEMATIC SIGNIFICANCE OF outbred populations. Also the impact of VARIATION IN CERION the new environment may lead to a drastic modification of the contents of the gene pool in the new population and conse- Bimini Islands quently in the phenotype" (Mayr & Rosen, 1956: 43). They emphasize that this great

Ernst Mayr's detailed study of the morphological plasticity is an adaptation to cerions of the Bimini Islands in the Ba- the pioneer habitat in which Cerion lives: a hamas constitutes the first notable contri- habitat which changes continuously as a bution to the evolution of Cerion con- result of eustasy, plant succession, and ducted in a modern framework (Mayr & natrual catastrophes. Rosen, 1956). Their conclusions are worth On the one hand Mayr & Rosen saw noting here as they indicate the intracta- Cerion as an actively speciating group and bility of the Cerion phenomenon and set on the other, as an extreme example of the stage for our own work. Mayr con- reticulate evolution on the intraspecific ducted a very careful survey of the cerions level. They concluded that the very char- of the six small islands in this group and acteristics (variation in shell morphology) found geographic variation to be pro- which have adapted these snails so superbly

nounced but irregular. While each colony to the habitat in which they live made it had its own diagnostic features, three major impossible to classify them in terms of the morphotypes were recognizable. These cor- conventional categories of species and sub- responded to the species lerneri, species. 230 WOODRUFF Dutch Leeward Islands Variation within each island or geographic area appears to be influenced by The type-species, uva, was described environmental parameters. Surprisingly, the by Linnaeus in 1758. It is restricted to the Cerion collected from volcanic areas on islands of Curaçao, Aruba and Bonaire Curaçao have larger shells than those found which lie off the coast of Venezuela and on limestone. This anomaly is probably not some 800 km south of the rest of the range related to the substrate itself but to the of the genus. In marked contrast to the microenvironmental features usually associ- situation in Cuba and the Bahamas only a ated with it. On Curaçao the limestone single variable species was recognized by areas are typically very dry, windswept and the early conchologists. Gould resolved to poorly vegetated; the volcanic areas are begin his study of the genus with this more sheltered and have a more mesic single, isolated taxon before confronting vegetation. Baker (1924) was the first to the more complex situations elsewhere. He notice an inverse relationship between the was originally attracted to Cerion because number of whorls (and shell height) and it provided all the features he could enu- the degree of exposure to the dry trade merate for an ideal biometrical subject. winds. He suggested that the evaporative First, adequate sample sizes are almost effect of the wind reduced the snails' ac- never a problem. Second, Cerion shows a tivity period and hence its adult size. clear and sharp transition between the Gould found additional support for this protoconch and later accretionary growth. hypothesis: plotting mean shell height for This provides a criterion for the numbering 15 samples he collected from similar micro- of whorls as a reference for standardized habitats on the first terrace along the measures at various stages of ontogeny. northern coast of Curaçao he found that Finally, and unlike most snails, Cerion shells were largest where the coast runs due changes its direction of growth near the east-west and the trade winds do not blow end of ontogeny and secretes a single, directly on shore. Elsewhere, where the permanent adult lip. The bugbear of most coast runs north-south the shells are smaller biometrical studies of molluscs lies in the (Gould, 1971: fig. 46). Coincidentally, the difficulty (if not impossibility) of sorting area where the coast runs east-west is also ontogenetic from static adult variation. the area of volcanic soil. Still other evi- This can be done unambiguously in Cerion dence for environmental selection for shell and we can assess the true standardized size comes from fossil samples from Aruba variance of adult shells. and Curaçao. Gould (1971) found that C. uva offered one other attraction: it shells from three middens on Curaçao dat- is among the world's best known land ing to about 4000 y BP were larger than snails from a biometrical point of view. It any living on this island today. Larger had been the subject of two major studies shells were also found in a midden on (Baker, 1924; Hummelinck, 1940; see also Aruba dated at 1500 y BP. Gould argued De Vries, 1974). Gould began by reanalyz- that this suggests that the island's climate ing the published data for a series of 102 was moister during these periods than at samples well distributed over the three present. If these interpretations are correct islands. In contrast to earlier workers he then the phenotypic variation within this applied a variety of multivariate statistical single species is continuous rather than techniques to elucidate patterns of intra- capricious and adaptive rather than adventi- and intersample variation (Gould, 1969). tious. He found an excellent correspondence between the data of Baker and Hummelinck Little Bahama Bank on interregional diversity; samples sorted into four groups corresponding to Aruba, Bonaire, Gould and I began our collaborative eastern and western Curaçao. Diversity pat- field work on the northernmost Bahamian terns did not change significantly during the bank: the Little Bahama Bank consisting of 16 years between these studies. Next, Gould Grand Bahama, Little Abaco, Great Abaco compared the early samples with a series of and their fringing islands. This area was 69 modern samples he made himself (see blessedly spared from visits by Maynard, Gould, 1971: unpublished data for mono- one of the most exuberant conchological graph in preparation). Again, the patterns do splitters to focus on this genus, and re- not change over the 50 year period. ported diversity was only 12 species. These NATURAL HISTO RY OF CERION 231 names, plotted in the supposed areas of revision of the genus, we predict that the their occurrence, produce the "crazy-quilt" number of species of Cerion may be re- distribution pattern traditionally associated duced almost 100-fold. with Cerion (Gould & Woodruff, 1978: fig. We have subsequently extended our 1). After several trips to these islands it study to the Cerion of the entire bank and became clear, however, that the dozen or have been able to resolve a pattern involv- so names refer to two variable and imper- ing two variable semispecies (Gould & fectly isolated taxa (Gould & Woodruff, Woodruff, 1978). It turns out that 1978). These semispecies, bendalli abacoense is restricted to those present-day (smooth or finely ribbed and mottled shell) coasts which lie close to the edge of the and abacoense (heavily ribbed white Little Bahama Bank. We will refer to it as shell) are shown in Figs. 2, 3). being a "bank edge" species. In contrast, C.

This taxonomic simplification was not, bendalli is a "bank interior" species, found however, immediately obvious to us as in the interior of the islands and on coasts both species show considerable geographic washed by the very shallow waters covering variation. On our first survey trip, for the bank today. In southern Great Abaco, example, we discovered a local situation the geography of the present-day coast where a population of Cerion bears a mor- relative to the edge of the bank is such phology sufficiently distinctive to warrant that there are several places where the recognition as a new species by all previous ranges of these 2 morphotypes come into criteria. Our resolution of the taxonomic contact and hybridization occurs. To re- status of this aberrant population, from solve the patterns of variation in each Pongo Carpet on the northeast coast of morphotype and to investigate the nature Great Abaco, provided us with an oppor- of their interaction we studied variation in tunity to test our combination of multi- 20 shell characters and 28 genetic loci in variate morphometric and biochemical over 50 samples from across the bank. genetic techniques (Gould et al., 1974). Morphometrically, the two morphotypes

This population is semi-isolated by man- may be sorted unambiguously by factor groves on a narrow coastal strip and is in analysis; 3 factor axes encompass over 96% contact with other populations only in the of the information. All samples from the north. Its morphology is highly distinctive area where the two taxa meet plot in the (see Gould et al., 1974: fig. 3) but its intermediate phenetic field: the hybrids patterns of covariation (as revealed by fac- have intermediate phenotypes. Near Rocky tor analysis) cannot be distinguished from Point the zone of allopatric hybridization those of bendalli within whose range it (sensu Woodruff, 1973) is 1 km wide and occurs. These patterns of covariation there is a gradual transition in mean mor- among the 19 variables measured were, phology across the zone with no increase in however, impressively different from those intrasample variability.

which characterize C. abacoense which is My study of allozyme variation for the found 70 km away at the southern end of same snails revealed very little concordance the island. Canonical analysis revealed a between the genetic and phenetic patterns. multivariate dine extending from Pongo All samples of both C. bendalli and Carpet north towards the area of potential abacoense are markedly similar: Nei's contact with typical C. bendalli. Levels of genetic identity (I) for 820 pairwise com- morphological variability did not differ parisons averaged 0.98. No unique marker among samples; those of intermediate mor- gene characterizes any region or morphology show no increase (or decrease) in photype, though characteristic frequencies variability or other signs of hybridity. Elec- of certain variable alleles clearly separate trophoresis showed the Pongo Carpet Grand Bahamian from Abaconian Cerion in Cerion to be genetically indistinguishable a statistical manner. Despite this overall from C. bendalli at the 18 structural gene genetic similarity the pattern of allozyme treat the loci surveyed. I could find no evidence for variation supports our decision to any genetic anomaly within the 12 popula- Little Bahama Bank Cerion as two semi- tions (7 from Pongo Carpet) sampled from species. Although hybrids showed no in- northern Great Abaco. We concluded that crease in morphometric variability they the Pongo Carpet Cerion are only a well- showed significantly more genetic vari- marked geographic variant within ability (both within and between popula-

bendalli. If this situation is any model for a tions) than snails collected elsewhere. They 232 WOOD RUFF are also polymorphic for alleles not de- Nassau) has been scoured for Cerion for tected in either adjacent "parental" popula- over a century and 82 species have been described from this relatively small island tion. I have now resampled this hybrid zone and a more detailed discussion of its (207 km^). Yet we quickly realized that significance will be presented elsewhere the situation here was very similar to the (Woodruff & Gould, in prep.). pattern we had elucidated on the Little

It should be clear from the above discus- Bahama Bank. There are two imperfectly sion that there is no evidence that the separated entities: a ribby abacoense-Wke various colonies of Cerion on the Little form (called g/ans on this island, see Fig. Bahama Bank were founded by single hur- 4) and a mottled bendalli-Wke form (whose ricane-transported waifs. The very high correct name we have yet to establish). genetic similarity among the various pop- Again, the ribby morphotype is a "bank ulations sampled suggest that hurricanes edge" species found on the western edge of have not played a significant role in the the island and on the offshore cays. The recent evolution of these snails. The situa- mottled morphotype inhabits the interior tion may be quite different on the tiny of the island and the eastern and southeast- offshore cays surrounding the main islands; ern coasts on the "bank interior" side of interaction between unfortunately I have not yet been able to the island. The zone of is, however, different study them genetically. I have, however, these morphotypes studied variation in populations of C. from that described on Abaco. While multi- bendalli from Snake and Tuggy Cays which variate dines mark the east-west transition are adjacent to Great Abaco (Woodruff, across this island the hybrid zone is char- 1975b). These populations show the same acterized by novel phenotypes and by un- amount and type of genetic variation as the usual intrapopulation variation in shell size. adjacent populations from the main island. There is no smooth continuity of pheno- of pheno- Again, there is no evidence that these type, but rather a host mixed populations were derived from single types. This is borne out in a Q-mode factor founding individuals. For the Little Bahama analysis: the hybrid population is character- Bank Cerion we reject the notion that the ized by shells which secrete the adult lip the character- pattern is a "crazy-quilt" due to hurricane- abruptly, without undergoing dispersed morphotypes. Instead we con- istic changes in the axis of coiling typical the clude that the pattern is quite coherent and of all other cerions. Genetically, two evolved at a time when sea levels were morphotypes on New Providence are very lower and the populations on the various similar, as they were on Abaco. On New islands were in full genetic contact with Providence, however, the transitional popu- each other. lations are not distinguished by any genetic anomalies. A paper in which we will sub- Great Bahama Bank sume 80 taxa and describe the nature of the variation in these two semispecies and Following our study of the Cerion in the significance of their interaction is now the northernmost Bahamian group of being prepared. islands we turned our attention to the far We have made one survey trip to the more complex situation on the Great Exumas and found, once again, that despite Bahama Bank. Here, there are a number of the plethora of available names there are large islands (Andros, New Providence, basically two contrasting morphotypes pres- Eleuthera, Cat, Exuma and Long), numer- ent. There are numerous varieties of a ous small cays and several hundred de- bendalli-Wke mottled form (for which C. scribed species. In the last five years Gould eximeum may be the oldest available name) Little Exuma and on the and I have undertaken exploratory surveys on Great and on all the main islands (collecting both innumerable cays in the Exuma chain. living and fossil Cerion) and examined ma- There is a ribby abacoense-Wke form on terial in the collections of the major U.S. some of the cays which lie close to the museums. Our studies on three of the large edge of the bank. Only two forms depart of these islands have reached the stage where I can dramatically from one or other announce some of our preliminary findings; morphotypes. One, pauli (Fig. 6) from detailed reports will be published else- Great Exuma, matures at less than half the where. typical size of the mottled forms but has New Providence (with the city of 10-12 whorls, or 2-3 more than normal. We NATURAL HISTO RY OF CERION 233 have no reason to regard it as anything not simply due to more intensive sampling more than a strongly dwarfed population of the intermediate populations. We see the of the mottled morphotype. It is also elucidation of the genodynamics of these atypical in its habits, being found in piles hybrid zones as important to the under- of rotting vegetation near the mangroves standing of the process of evolution of on the "bank interior" coast. The other Cerion. In particular we will attempt to aberrant type is an isolated population of a establish whether the zones are of primary member of the subgenus Umbonis on Great or secondary origin or whether they are a Guana Cay. Museum specimens indicate mixed group. It strikes us that marked that this population, which was presumably geographic differentiation and parapatric derived from Cuba, is hybridizing with the speciation are quite possible in a group like local mottled forms. Cerion. Interestingly, parts of the complex On Long Island, at the southeastern distribution pattern on Long Island are edge of the Great Bahama Bank, we found relatively old; fossils indicate that some of that our simplifying generalization about these species have been in place for at least "bank edge" and "bank interior" morpho- 110,000 years. types was complicated by the incursion of several additional morphotypes. A few of Florida Keys the species described from Long Island are shown in Figs. 7-13. In the course of 3 A single endemic species, incanum, field trips to this island we have mapped occurs in the Florida Keys and north as far the distribution of these forms and uncov- as Key Biscayne in Miami. It is a medium- ered by far the most interesting situation sized, typically smooth-shelled species and that we have yet encountered in Cerion. has little geographic variation (Fig. 5). I

First, we discovered that two basic mor- have recently discovered that, unlike all photypes were present: a mottled form, other Cerion examined, incanum is large- eximeum, occurs along the western "bank ly invariant genetically. All the populations interior" coast and a strongly ribbed form, sampled in the Keys (sensu stricto) to date caerulescens, occurs on the eastern coast are monogenic; samples from Key Biscayne adjacent to the edge of the bank. In addi- were polymorphic at an esterase locus. This tion we found five other distinctive mor- contrasts markedly with the situation in photypes along parts of the hilly east coast. Cerion from the Bahamas, Puerto Rico and These taxa replace one another along the Curaçao which are typically polymorphic at coast and we have now located 12 narrow 4-6 loci. In this respect incanum is more hybrid zones between various combinations like North American populations of of these forms. Particularly spectacular Rumina decollata than any other zones involve the large, white, smooth- pulmonale gastropod described to date shelled fernandina, the squat, white, (Selander & Kaufman, 1973, 1975a). We smooth-shelled malonei, and the dis- will use this observation to standardize the tinctive member of the subgenus Umbonis, nomenclature for the allozymes detected in Stevenson! (Fig. 12). Defined on the Cerion (Woodruff & Burgess, in prepara- basis of shell morphology these hybrid tion.) Henceforth, different allozymes will zones are quite narrow (some are only be compared directly to those in C. incanum 100 m wide), and may or may not be and designated by their quantitative relative associated with marked changes in abun- mobility. dance or habitat. While the various species Gould and I made a second exciting involved in these interactions are very simi- discovery in the Florida Keys. In 1911 Paul

lar to each other genetically I found that Bartsch began a series of transplantation at least two of the hybrid zones are char- experiments aimed at showing that snails acterized by significantly greater fluctua- moved to a new environment would rapidly tions in interpopulation allele frequencies evolve to resemble the local (and pre- and by the presence of novel genotypes sumably optimal) Cerion morphotype. He absent from adjacent "parental popula- transplanted several samples of Bahamian tions." Michael Goldman, in my laboratory, cerions to the Dry Tortugas and other Keys has carefully checked intersample variation (Bartsch, 1920). Fires, hurricanes and other in adjacent populations away from one of setbacks marred the experiments and the these hybrid zones (fernandina-stevensoni) transplants bred true to their ancestral to ensure that our preliminary findings are phenotype for as many generations as he 234 WOOD RUFF could follow. He concluded that pheno- Museum of Comparative Zoology and pre- typic variation in Cerion is not under strict pared distribution maps of the purported environmental control. As some of his taxa. The resolution of the resulting com- transplants hybridized with the resident plex patterns will require additional field incanum, and as the hybrids were "enor- work. mously variable" (a phenomenon Bartsch In the 1950's Ernst Mayr collected attributed to mutation), he further con- Cerion in Cuba and his distribution map of cluded that the "crazy-quilt" pattern of forms on the Banes Peninsula on the north- geographic variation in this genus was ad- eastern coast has done much to draw atten- ventitious rather than adaptive (Bartsch, tion to the genus and its problems (Mayr, 1949). While Bartsch's experiments were 1963:398-399, 1969:17, 1970:33). In inadequate to assess the process of local this area Mayr found 7 highly distinct adaptation, and while his ideas of "mutat- morphotypes replacing each other geo- ing hybrids" as the source of Cerion's graphically along a 50 km stretch of coast. diversity, are not supported by modern Within four zones of contact presenting no genetic theory, we are indebted to him for ecological barriers to effective gene flow, initiating these experiments nearly 60 years he found populations which he interpreted ago. We have discovered that the descend- as the hybrid products of secondary inter- ents of one of his transplantations still gradation. Lynne Caller and Gould (in flourish today in a restricted area at the prep.) have been studying the narrow tran- site of the original introduction. The in- sition zone between two of the most diver- troduced species hybridizes with C. gent morphotypes: morales! and incanum and the hybrids continue to show geophilus. Their biometrical studies show a range of variant phenotypes and a general no increased variability in the geographical- level of variation far higher than that seen ly intermediate samples. Several univariate in homospecific populations. Bartsch docu- and a multivariate dine cover the zone mented the early stages of his experiments which is less than 1 km wide. They find in great detail and it has been possible to that the large morphological differences be- re-collect from the original Bahamian tween these taxa may arise from a small source population and confirm their alteration in the rate of shell widening identity genetically. We will describe this during the early phase of post-embryonic interesting experiment and discuss its evolu- growth. The interplay of this simple event tionary implication in the near future. with the complex allometries of normal ontogeny produces the large adult dif- Isolated Bahamian banks ferences. We must now confront the fascinating question: can any Cerion be We have had limited field experience transformed into any other by simple with the cerions on a number of the heterochronous changes in early ontogeny? smaller island banks: San Salvador, Inagua, Rum and Conception. Rum Cay and Con- Hispaniola, Puerto Rico and the ception Island lie on small, isolated banks Virgin Islands to the north and east of Long Island. Each is inhabited by a single, variable species of Gould and Pauli (1977) completed a the ribby morphotype. Kathleen Ligare and study of Cerion from the eastern end of its

I are establishing the genetic and phenetic range: Hispaniola, Mona Is., Puerto Rico, relationship between these snails and the and Necker and Anegada in the Virgin

similar morphotypes on Long Island from Islands. Here 1 1 names were available for a which they might have been derived. basic morphology that all students of Cerion have recognized as unique to this Cuba area (Pilsbry, 1901-1902). They performed a canonical analysis of morphological varia- The north and eastern coasts of Cuba tion in 23 samples from throughout this are perhaps the center of Cerion's remark- area and found that these samples are able diversity. We have begun a revision of arranged along the most significant dis- this large island's rich fauna; 147 "species criminator (the first axis: 59% of all infor- and subspecies" according to Clench (1957) mation) in perfect geographic order. The and Jaume (1975). We have examined all morphological gradient runs from egg- specimens in the great collection at the shaped, finely and copiously ribbed shells NATURAL HISTO RY OF CERION 235 with very obtuse apices (Virgin Islands) to analogy to the situation in Cepaea—a prob- more cylindrical, apically-pointed shells lem with too many solutions (Jones et al., with fewer, stronger ribs (Hispaniola). In 1977)— is striking. the light of this clinal pattern they reduce In the interim, how are we to regard all available names to a single species, C. these markedly different populations? Are stria te//urn. they ecotypic races, morphospecies, or biological species? At present we think Cerion may comprise a number of variable and DISCUSSION polytypic semispecies. The actual number of these taxa is not yet known but we Prior to the commencement of our work agree with Clench's (1957) opinion that three major attempts were made to inter- perhaps only 20% of the described species

pret Cer/on's complex diversity. Plate are valid. I emphasize that we still know (1906, 1907) argued that the variation in nothing about reproductive isolating mech- shell morphology was adaptive. His inter- anisms in Cerion; statements to the effect pretation was in a Lamarckian mode, how- that reproductive isolating mechanisms are ever, and was based on very limited per- not easily acquired in this genus are based sonal experience with the animals and solely on the observation of shell types much misinformation about areas he had that are intermediate between various pairs not seen. Bartsch (1920, 1949) concluded of morphotypes. Until we identify the po- that the pattern was not adaptive and tential pre- and post-mating isolating mech- resulted from chance events (colony extinc- anisms and learn more about the reproduction and long-distance dispersal), evolution tive anatomy and behavior of various in isolation, and subsequent diversification cerions, we simply cannot comment on the among "mutating hybrids." Mayr (1963; significance of the alleged interspecific dif- and Mayr & Rosen, 1956) interpreted the ferences. For example, we still do not variation as adaptive but also argued that know whether selfing plays any role in stochastic events play an important role in Cerion's mating system (as it does in early the development of the overall pattern. reproductive life in Partula taeniata (Mur- Mayr regarded each colony as an evolution- ray & Clarke, 1976)). Working in my labo- ary experiment whose ultimate fate is in- ratory, Daniel Chung has taken on some of determinate. He interpreted the "crazy- these fascinating problems. quilt" distribution pattern in terms of local The lack of marked genetic differences extinction and recolonization with sub- between the various cerions studied has sequent secondary contact between con- little bearing on speciation per se. Twelve trasting morphotypes dispersed primarily years of biochemical genetics of many or- by storms. He repeatedly cites Cerion as ganisms provides little evidence for exten- the classic example, in animals, of the sive reorganization of gene pools during acquisition of morphological differences speciation (Throckmorton, 1977). There is without reproductive isolation (Mayr, 1963, every indication that changes in a few loci 1969, 1970). are sufficient for speciation and that geo-

In the past few years Gould and I have graphic variation rather than genetic revolu- personally confronted about one third of tion may be the critical prerequisite.

the alleged diversity in Cerion. Our combi- As I can demonstrate no major differ- nation of laboratory studies employing entiation in structural genes among the multivariate morphometric and biochemical most widely divergent of Cerion's morpho-

genetic techniques is proving successful. types we are forced to look elsewhere for Given time we have every reason to believe the underlying genetic determinants. Gould that Cerion's taxonomic overburden will be (1977) has argued that complex differences removed and the evolution and adaptive in form can often be traced to simple radiation of these snails can be exposed for differences in developmental rates ex-

direct investigation. While it should be clear pressed during ontogeny. Since these rates

that our bias is towards an interpretation are probably controlled by regulatory genes involving both history and adaptation it is (King & Wilson, 1975) it is not surprising clear that we have not yet reached the that allozymic (structural gene products)

point where sweeping generalizations are variation is small. The possibility that possible. It turns out that the earlier work- minor developmental changes will translate ers were partly right and partly wrong; the into major differences in adult morphology 236 WOOD RUFF is strongly enhanced in Cerion by the com- in microhabitat, shell function, and the plex allonnetries that characterize growth: mechanics of crawling (see Cain, 1977; and particularly the 3 divergent phases of juven- papers by Cain and Linsley in this sympo- ile triangularity, mid-growth "barrelling," sium). In Cerion the spire index (height/ and adult recurvature. Our vision is to max. diameter) of juvenile shells is 0.5-0.7; reduce all this diversity to a simple system in adults the index is typically above 3.0 of ontogenetic growth gradients and their and can be as high as 7.0. Juveniles are quantitative alteration. We have also tried typically found on the ground surface be- to develop a "dynamic" approach to de- neath the leaf litter and are usually ori- scribing shell variation and choose to work ented apex up. In contrast, the adults are with patterns of covariation rather than invariably found hanging on plants apex static adult morphology. Our initial experi- down. Lip size appears to be correlated ences have been most promising and it is with habit and habitat: small lipped shells pleasing to note that the raw data pre- are often associated with grass or leaf litter sented in our first paper (Gould et al., in humid microhabitats; cerions with large 1974) has already been used as a basis for recurved lips are associated with drier areas two subsequent studies (Sokal, 1976; which are exposed to the prevailing wind Schueler & Rising, 1976). To give our and often have rocky substrates. It is pos- enormous data sets even greater validity sible that the greater surface area of an Kathleen Ligare has recently completed a aperture with a large lip give the shells study of the measurement errors associated (which is fastened to the substrate or vege- with each morphometric trait. tation by a thin epiphragm) greater stabil-

ity in windy situations. I can not comment So far I have not discussed the possible adaptive significance of the variation seen yet on the possible significance of variation in teeth are present in in Cerion. I proceed into the difficult field the apertural which of functional morphology with Darwin's most cerions in both juvenile and adult remarks (quoted by Cain, 1954) on the phases. Shell sculpture or ornamentation is danger of believing apparently trivial char- another variable character of unknown acters to be of no functional importance adaptive significance. While in some areas and in no way due to natural selection ribbing appears to be correlated with hu- firmly in mind. It is not at all surprising midity and with the presence of a calcare- that earlier workers, confronted with the ous substrate, in other areas this generaliza- puzzling and apparently random distribution does not hold. John Ouensen, in my tion of morphotypes, gave up and decided laboratory, is examining Vermeij's (1975) that the pattern was due to drift and other suggestion that ribbing is an adaptive re- random processes. It is only from our sponse to predator pressure in snails since experience with Cerion in nature that we prominent ribs confine the predator's feel emboldened to ask questions about the crushing force to the thickest part of the adaptive significance of variation in the shell. His preliminary results indicate that shells and other features. overall shell size (weight and height) is We have reached the stage where we can more important than ribbing in determining speculate about the possible adaptive sig- a cerion's ability to withstand crushing nificance of variation in shell size, shape, forces applied generally along the sides of sculpturing and color. We proceed by look- the shell. He is now repeating these experi- ing for obvious correlations between mor- ments using artificial crab chelae to apply phometric traits and environmental para- forces at right angles to the shell's long meters. Overall shell size, for example, ap- axis; a more realistic design in view of our pears to be correlated with humidity and findings at Rocky Point. Ouensen has also the degree of shelter from the wind on been considering the possible adaptive sig- Curaçao. Unfortunately, this trend does not nificance of shell pigmentation. Mottled seem to explain patterns on the Great shells are initially hard to find as they hang Bahama Bank where even greater inter- on bush stems and blades of grass in the population variation occurs on single dappled sunlight and shadow, a clear case islands. Dwarfing occurs in some popula- of disruptive coloration to our eyes (Gould tions of most of the main morphotype & Woodruff, 1978: fig. 4). In contrast, in the vegeta- groups. I note that juvenile and adult shells white shells are conspicuous are quite different in shape and wonder if tion (see Bartsch, 1968: fig. 24). Ouensen this might be correlated with differences found that when shells are compared be- NATURAL HISTO RY OF CERION 237 neath a heat lamp in the laboratory the occupies an area that is large relative to the interior of a mottled shell averages at least gene flow distance and close evolutionary 1°C warmer than the interior of an unpig- "tracking" of microenvironmental hetero- mented shell. In the Bahamas he found the geneity is a real possibility. I am now effect of differential heating to be even beginning to look for evidence of this at greater: up to 4°C differences in Novem- the study sites on Abaco. The measurement ber, the actual difference being propor- of natural selection operating on various tional to the air temperature. As the upper traits in nature is quite difficult; our initial lethal temperature for Cerion is about approach involves looking for asymmetry in

52.5°C it is quite possible that a pigmented the various biométrie traits. I am also ex- shell exposed to the summer sun risks tending my investigation of gene flow to thermal death. The occurrence of unpig- assess its magnitude in low (rather than mented shells in exposed coastal situations high) density populations. Cerion provides may be a thermoregulatory adaptation. prime material for the experimental investi- We cannot even begin to discuss the gation of natural clines and hybrid zones. possible adaptive significance of variation in Land snails are well suited to studies of characters other than those associated with evolution and adaptive radiation (Clarke et the shell. Alleged interspecific variation in al., in press). The lessons of Cepaea (re- the radula and reproductive system are not viewed by Jones et al., 1977), Theba pisana adequately documented. Similarly, we can (Hickson, 1972; Nevo & Bar, 1976) and not yet account for the distribution of the Helix pomatia (Pollard, 1975; Järvinen et snails themselves. Their absence from al., 1976) on the role of natural selection Jamaica and the Lesser Antilles is puzzling. and other agents in the microevolution of Even within the areas where they occur we natural populations are particularly note- have no adequate theory to account for worthy. Studies of the variation of Partula Cerion's microdistribution. Even the most in the Society Islands resulted in significant basic assertions that cerions are halophiles contributions to the theory of clines and (Mayr, 1963) or calciphiles (Clench, 1957) parapatric differentiation (Clarke, 1968; are contradicted by the occurrence of snails Clarke & Murray, 1969; Murray, 1972). up to 15 km from the coast on Grand These studies, and others which focus on Bahama and in volcanic (non-limestone) other organisms with low vagility, cast in- areas on Curaçao. creasing doubt on the universality of the Cerions are remarkably like some vari- allopatric model of speciation (Bush, 1975;

able plants, in which spectacular examples Endler, 1977; Woodruff, 1978). Finally, I of highly localized, specially adapted eco- note that recent work on genie variability types which replace one another over dis- and breeding systems in Helix aspersa and tances of a few meters are well known Rumina decollata (Selander & Hudson,

(Bradshaw, 1972). I see considerable prom- 1976; Selander & Kaufman, 1973; 1975a; ise in attempting to reinterpret some of the 1975b) have implications for evolutionary patterns within the context of a model of ecology far beyond the confines of mala-

parapatric differentiation rather than the cology. It is our hope that Cerion will take allopatric model advocated by Mayr its place among this small group of land

(1963). This is necessary because recent snails that are of major significance to theoretical work on dines (Endler, 1977; biology generally. Woodruff, 1978) indicates that the traditional criteria used to distinguish between primary and secondary intergradation are REFERENCES CITED inappropriate. We must carefully examine aspects the possibility of explaining some BAKER, H. ., 1924, Land and freshwater mol- of the Cerion pattern in terms of con- luscs of the Dutch Leeward Islands. Occa- temporary selection gradients and dispersal sional Papers of the Museum of Zoology, University of Michigan, 152: 1-158. patterns. A continuously distributed popu- BARTSCH, P., 1912, Planting Bahama cerions 10^-10^ lation of snails cannot be con- upon the Florida Keys. Yearbook of the sidered as though it were a single random Carnegie Institute of Washington, 11:

mating population; Cerion is apparently 129-131. BARTSCH, P., 1920, Experiments in the breeding broken up into small demes containing of cerions. Papers of the Department of 10^ approximately individuals. Each deme, Marine Biology, Carnegie Institute of Washing- even those in a more extensive population. ton, 282: 1-55. 238 WOODRUFF

BARTSCH, P., 1949, Molluscan genetics: the role GOULD, S. J., 1969, Character variation in two of hybridization, nnutation, isolation, fixation land snails from the Dutch Leeward Islands: and speciation in relation to taxonomy. Amer- geography, environment, and evolution. Sys- ican Malacological Union News Bulletin and tematic Zoology, 18: 185-200. Annual Report, 1948: 2-A. GOULD, S. J., 1971, The paleontology and evo- BARTSCH, P., 1968, Mollusks. (Republication of lution of Cerion, II: age and fauna of Indian Smithsonian Institution Series, 10(3), 1934.) shell middens on Curaçao and Aruba. Dover, New York, 111p. Breviora, 372: 1-26. BRADSHAW, A. D., 1972, Some of the evolu- GOULD, S. J., 1977, Ontogeny and phytogeny. tionary consequences of being a plant. Evolu- Belknap Press of Harvard University Press, tionary Biology, 5: 25-47. Cambridge, 506 p. BURCH, J. B. & KIM, D. C, 1962, Chromosomes GOULD, S. J. & PAULL, C, 1977, Natural of Cerion incanum (Binney) (Mollusca: history of Cerion. VII. Geographic variation of Gastropoda: Stylommatophora). Bulletin of Cerion (Mollusca: Pulmonata) from the east- the National Institutes of Health (Korea), 5: ern end of its range (Hispaniola to the Virgin 181-186. Islands): coherent patterns and taxonomic BUSH, G. L., 1975, Models of animal speciation. simplification. Breviora, 445: 1-24. Annual Review of Ecology and Systematics, GOULD, S. J. & WOODRUFF, D. S., 1978, 6: 339-364. Natural history of Cerion. VIM, Little Bahama CAIN, A. J., 1954, Animal species and their Bank— a revision based on genetics, morpho- evolution. Hutchinson, London, 190 p. metries and geographic distribution. Bulletin CAIN, A. J., 1977, Variation in the spire index of the Museum of Comparative Zoology, 148. of some coiled gastropod shells, and its evolu- GOULD, S. J., WOODRUFF, D. S. & MARTIN, tionary significance. Philosophical Transactions J. P., 1974, Genetics and morphometries of of the Royal Society of London, ser. , 277: Cerion at Pongo Carpet: a new systematic 377-428. approach to this enigmatic land snail. System- CLARKE, ., 1968, Balanced polymorphism and atic Zoology, 23: 518-535. regional differentiation in land snails. In: HICKSON, T. G. L., 1972, A possible case of DRAKE, E. T. (Ed.), Evolution and Environ- genetic drift in colonies of the land snail ment. Yale University Press, New Haven, p. Theba pisana. Heredity, 29: 177-190. 351-368. HUMMELINCK, P. W., 1940, Mollusks of the CLARKE, ., ARTHUR, W., HORSLEY, D. T. & genera Cerion and Tudora. Studies of the PARKIN, D. T., in press. Genetic variation Fauna of Curaçao, Aruba, Bonaire, and the and natural selection in pulmonate molluscs. Venezuelan Islands, 2: 43-82. (Manuscript for publication in: FRETTER, V. JAENICKE, J. H., 1933, Untersuchungen zur & PEAKE, J. (Eds.), Pulmonates. 2: System- Anatomie und Verschiedenartigkeit der Cerion atics, evolution and ecology. Academic Press, Arten der Bahamas als Beitrag zum Problem London). der Artentstehung. Jenaische Zeitschrift für CLARKE, B. & MURRAY, J., 1969, Ecological Medizin und Naturwissenschaft, 68: 277-402. genetics and speciation in land snails of the JÄRVINEN, O., SISULA, H., VARVIO-AHO, genus Partula. Biological Journal of the S-L. & SALMINEN, P., 1976, Genie variation Linnaean Society, 1: 31-42. in isolated marginal populations of the Roman CLENCH, W. J., 1938, Land and freshwater snail. Helix pomatia L. Hereditas, 82: mollusks of Grand Bahama and the Abaco 101-110. Islands, Bahama Islands. Memorias de la JAUME, M. L., 1975, Catalogo de los moluscos Sociedad Cubana de Historia Natural, Museo terrestres Cubanos del genero Cerion (Mol- Poey, Universidad de la Habana, 12: 303-333. lusca-Pulmonata-Ceriidae). (Con una bibli- CLENCH, W. J., 1957, A catalogue of the ografía general.) Catalogo de la Fauna Cubana, Cerionidae (Mollusca-Pulmonata). Bulletin of 37. Ciencias, ser. 4, 51: 1-47. the Museum of Comparative Zoology, 116: JONES, J. S., LEITH, B. H. & RAWLINGS, P., 121-169. 1977, Polymorphism in Cepaea: a problem CLENCH, W. J. & AGUAYO, . G., 1952, The with too many solutions? Annual Review of scalarinum species complex {Umbonis) in the Ecology and Systematics, 8: 109-143. genus Cerion. Occasional Papers on Mollusks, KING, M. & WILSON, A. C, 1975, Evolution Harvard University, 1: 413-440. at two levels in humans and chimpanzees.

DARWIN, C, 1859, On the origin of species. . . Science, 188: 107-116. John Murray, London. (Facsimile of the first MAY, R. M., ENDLER, J. A. & McMURTIE, R. edition published by Harvard University Press, E., 1975, Gene frequency ciines in the pres- Cambridge, 1964.) ence of selection opposed by gene flow. DE VRIES, W., 1974, Caribbean land molluscs: American Naturalist, 109: 659-676. notes on Cerionidae. Studies on the Fauna of MAYR, E., 1963, Animal species and evolution. Curaçao and other Caribbean Islands, 45: Belknap Press of Harvard University Press, 81-112. Cambridge, 797 p. ENDLER, J. A., 1977, Geographic variation, MAYR, E., 1969, Populations, species, and evolu- speciation and dines. Monographs in Popula- tion. Belknap Press of Harvard University tion Biology No. 10, Princeton University Press, Cambridge, 453 p. Press, Princeton, 246 p. MAYR, E., 1970, Principles of Systematic Zool- GALLER, L. & GOULD, S. J., in prep.. Continu- ogy. McGraw-Hill, New York, 428 p. ous phenetic transformation in a zone of MAYR, E. & ROSEN, ., 1956, Geographic interaction between two "species" of Cerion variation and hybridization in populations of in Cuba: the reduction of complex form to Bahama snails (Cerion). American Museum of simple generating factors in ontogeny. Natural History Novitates, 1806: 1-48. NATURAL HISTORY OF CEBION 239

MURRAY, J., 1972, Genetic diversity and natural ture in a colonizing land snail. Proceedings of selection. Oliver & Boyd, Edinburgh, 128 p. the National Academy of Science (United MURRAY, J. & CLARKE, ., 1976, Supergenes States), 70: 1186-1190. in polymorphic land snails. 1. Partula taeniata. SELANDER, R. K. & KAUFMAN, D. W., 1975a, Heredity, 37: 253-269. Genetic population structure and breeding NEVO, E. & BAR, Z., 1976, Natural selection systems. In: MARKERT, L. (Ed.), Iso- and genetic polymorphisms along climatic zymes, 4. Academic Press, New York, p. gradients. In KARLIN, S. & NEVO, E. (Eds.), 27-48. Population genetics and evolution. Academic SELANDER, R. K. & KAUFMAN, D. W., 1975b, Press, New York, p. 159-184. Genetic structure of populations of the brown PILSBRY, H. A., 1901-1902, Family Cerionidae. snail (Helix aspersa). I. Microgeographic varia- Manual of Conchology, ser. 2, Pulmonata, tion. Evolution, 29: 385-401. Academy of Natural Sciences of Philadelphia, SOKAL, R. R., 1976, The Kluge-Kerfoot 14: 174-286. phenomenon reexamined. American Naturalist, PILSBRY, H. A., 1946. Land Mollusca of North 110: 1077-1091. America. Academy of Natural Sciences of THROCKMORTON, L. H., 1977, Drosophila Philadelphia, Monographs 3, 2(1): 158-169. systematics and biochemical evolution. Annual PLATE, L., 1906, Die Artbildung bei den Cerion- Review of Ecology and Systematics, 8: Landschnecken der Bahamas. Verhandlungen 235-254. Deutschen Zoologischen Gesellschaft, Leipzig, VERMEIJ, G. J., 1975, Marine faunal dominance 16: 127-138, 1 pl. and moiluscan shell form. Evolution, 28: PLATE, L., 1907, Die Variabilität und die 656-664. Artbildung nach dem Prinzip geographischer WOODRUFF, D. S., 1973, Natural hybridization Formenketten bei den Cer/on-Landschnecken and hybrid zones. Systematic Zoology, 22: der Bahama-Inseln. Archiv fur Rassen- und 213-218. Gesellschafts-Biologie, 4: 433-470, 581-614. WOODRUFF, D. S., 1975a, A new approach to POLLARD, ., 1975, Differences in shell thick- the systematics and ecology of the genus ness in adult Helix pomatia L. from a number Cerion. Malacological Review, 8: 128. of localities in southern England. Oecologia, WOODRUFF, D. S., 1975b, Natural history of 21: 85-92. Cerion. V. Allozyme variation and genie hetero- RICHTER, ., 1926, Zur Anatomie von Cerion zygosity in the Bahamian pulmonale Cerion glans Küster der Bahamas-Inseln. Jenaische bendalli. Malacological Review, 8: 47-55. Zeitschrift für Medizin und Naturwissenschaft, WOODRUFF, D. S., 1978, Review of Geographic 62: 277-342. variation, speciation and dines by J. A. SCHUELER, F. W. & RISING, J. D., 1976, Endler. Science, 199: 1329-1330. Phenetic evidence of natural hybridization. WOODRUFF, D. S. & GOULD, S. J., in prep.. Systematic Zoology, 25: 283-289. Natural history of Cerion. XI. Genetics and SELANDER, R. K. & HUDSON, R. O., 1976, morphometries of the interaction between two Animal population structure under close in- semispecies of Cerion (Pulmonata) on Abaco, breeding: the land snail Rumina in southern Bahamas. France. American Naturalist, 110: 695-718. WRIGHT, S., 1946, Isolation by distance under SELANDER, R. K. & KAUFMAN, D. W., 1973, diverse systems of mating. Genetics, 31: Self fertilization and genetic population struc- 39-59.