The Demonstration of Speciation in Fossil Molluscs and Living Fishes

Biological Journal of the Linnean Society (1985), 26: 325-336. With 3 figures

The demonstration of speciation in fossil molluscs and living fishes

G. FR Y E R ,

Freshwater Biological Association, Windermere Laboratory, The Ferry House, Ambleside, Cumbria

P. H. GREENWOOD AND J. F. PEAKE

British Museum ( Natural History), Cromwell Road, London

Accepted for publication July 1985

Contrary to a recent assertion, freshwater (and marine) prosobranch gastropods and freshwater bivalves are subject to considerable variability. This, and the lack of a detailed understanding of the taxonomy of the forms involved, makes it difficult to accept that the changes documented by Williamson (1981) in a fossil sequence from Lake Turkana (Africa) represent speciation events. That 10 lineages, involving gastropods and bivalves, should change simultaneously, and the deviant forms should then simultaneously become extinct, can, we believe, be more plausibly attributed to ecophenotypic responses to environmental changes than to speciation. In revealing the pattern and process of evolution, both fossil and living forms are helpful, but in demonstrating the fine-scale events during and after speciation in living animals one can utilize techniques and observations that cannot be applied to fossil material. African cichlid fishes are particularly informative in this respect. Their current explosive radiation can be interpreted as a punctuational event in evolution.

KEY WORDS: —Speciation - ecophenotypic changes - fossil molluscs - fishes - Lake Turkana.

CONTENTS

I n tr o d u c tio n ...... 325 T he variability o f freshwater prosobranch g a s t r o p o d s ...... 326 Speciation or variatio n ...... 331 Living fishes, fossil molluscs and the dem onstration o f sp eciatio n ...... 333 C o n c lu s io n s ...... 335 References...... 335

INTRODUCTION While we admire the tenacity of Williamson in defending his interpretation of the assemblage of Caenozoic fossil molluscs at Lake Turkana against several critics, we are still unable to accept some of his conclusions, and find his defence against our criticisms (Fryer, Greenwood & Peake, 1983) unconvincing. Furthermore, by misinterpreting much of what we wrote he has brought up various points that are irrelevant to the general discussion.

Williamson treats our criticisms under three headings. First he seeks to maintain the fiction that phenotypic variation in prosobranchs is small. He says nothing about bivalves, though in fact six of the 10 lineages on which the conclusions of his original paper (Williamson, 1981) are based are bivalves. He thereby circumvents the need to refute the well-established ecophenotypic variability of this group, to which we drew attention, as did Kat & Davis (1983). Second, he defends his claim that the forms present at the Suregei level are new species and not simply ecophenotypes, and finally he attempts to refute the suggestion that simultaneous changes in 10 lineages may indicate phenotypic changes rather than speciation. His disagreement about the limitations of fossil evidence and the relative value of fossil molluscs and living cichlid fishes as indicators of speciation, and his discussion of the punctuated equilibrium model of evolution are separate issues and are dealt with towards the end of this paper. In our original critique of Williamson’s interpretation of the Turkana fauna we outlined four lines of argument which seem crucial to a discussion of this interesting problem. (1) The considerable variability in shell form exhibited by freshwater prosobranch gastropods and by freshwater bivalves. (2) The problem of establishing a stable and unequivocal classification for such groups of organisms which has any biological meaning other than describing shell morphologies. Here, a major limitation is the absence of any taxonomic account establishing a baseline for Williamson’s study. One is available in his thesis (Williamson, 1980) but this differs from that employed in his publication in Nature (Williamson, 1981). (3) The availability of an alternative hypothesis, namely that the variation exhibited by the Turkana fauna could be explained as ecophenotypic or as under simple genetic control and not as speciation. (4) The belief that extant fishes of African lakes provide a far better example of rapid speciation (a punctuational phase of evolution), and therefore of the punctuated equilibrium model, than do the fossil Turkana molluscs. It should be noted that at no stage did we provide a critique of the punctuated equilibrium model. We noted the difficulties inherent in rigid adherence to any entrenched view, whether punctuationist or gradualist, but did not criticize either.

THE VARIABILITY OF FRESHWATER PROSOBRANCH GASTROPODS A major objection to Williamson’s conclusions is that they are based to a large extent on a false premise, namely that variation in freshwater prosobranchs (and also bivalves) is not subject to environmental or simple genetic control. He therefore presumes that morphologically deviant populations at certain levels must represent genotypic divergence and, in turn, assumes this to be evidence of speciation. Those views are proclaimed unequivocally in his original paper (Williamson, 1981) in which the phenotypic stasis of the gastropods involved is stressed, and claims are made that, unlike basommotophorans, freshwater prosobranchs “are characterised by narrow phenotypic ranges [of morphological variability] in modern faunas”. It is maintained that this is “paralleled by the geographical stability of phenotype exhibited by their widely distributed modern representatives”, and “their current morphological stability SPECIATION IN FOSSIL MOLLUSCS 327

in a diverse range of modern environments”. This, it is proposed, precludes the possibility of phenotypic shifts reflecting any other phenomenon than speciation. In fact it is well established that these and other prosobranch molluscs are variable (see F ryer et al., 1983; Kat & Davis, 1983). Indeed, when discussing the species concept among the freshwater prosobranchs of Europe, Boeter (1982) refers to the taxonomic problems raised by “the exceptional variability of freshwater prosobranchs”. Coming from a student of living molluscs, and referred to in a context in no way concerned with this debate, this can hardly be considered an endorsement of Williamson’s claims. Variability among bivalves, to which we referred and cited references in our critique, is perhaps even easier to substantiate (e.g. Tevesz & Carter, 1980). Perhaps wisely, Williamson makes no attempt to refute what we stated there, though alleged speciation events in bivalves play an important part in his story. Williamson would distinguish two kinds of variability in prosobranchs. One is that defined by ‘Raupian’ parameters which are “generalized geometric descriptors of fundamental shell form”. Variations in shell size, thickness and colour, previously ignored, he now dismisses as “comparatively minor ecophenotypic variations” which he thinks are largely controlled by variations in water chemistry. “Major variations in fundamental shell geometry and sculpture” he believes “are not usually ecophenotypically varying characters in freshwater prosobranchs”. Central to his distinction between the two kinds of variability, between which we see no qualitative differences, is his a priori belief that changes in Raupian parameters are necessarily under genetic control, and must be associated with speciation. These assumptions are not established. They have been considered largely, but not solely, with reference to marine species by Vermeij (1980) in a paper significantly entitled ‘Gastropod shell, growth rate, allometry and adult size: environmental implications’. Here a wide range of evidence is presented for a relationship between growth rate and allometric changes in shell shape, with growth rate being markedly influenced by environmental factors. Probably most gastropods do not maintain a constancy of shell shape during growth. Quoting from Vermeij, “The effects of the environment on growth rate, shape, and colour of snail shells, and the postulated correspondence between growth rate and allometry, have obvious implications for gastropod systematics. Shell features may be so profoundly altered by the environment that the unwary taxonomist may regard variants as separate species when in fact the morphs are merely different phenotypes determined by different environmental regimes. The taxonomic question can be resolved only if the forms are grown reciprocally in each other’s environments”. This problem has been expanded in considerable detail by Gould and his co workers in a study of a highly variable genus of pulmonate land snails, Cerion (see Gould, 1984, for references). We appreciate that pulmonates are not prosobranchs, but the principles are the same. Although Gould does not employ Raupian parameters he undertakes multivariate morphometries to investigate complex changes in shell shape. He poses the pertinent question “How are the remarkable differences in form produced and what do they mean?” He continues “The key insight must be D’Arcy Thompson’s favourite theme— that apparent differences in adult form are generated by complex consequences of small changes in ontogenetic pattern”. It is precisely for these reasons that molluscan taxonomists, who require high levels of resolution when 328 G. FRYER ETAL. characterizing taxa, have employed biochemical and cytological techniques to elucidate “the species problem”. In this context, criticism by Williamson of our failure fully to understand the meaning of the phrase “reorganisation of fundamental shell geometry” would seem rather inappropriate. More recently, and with specific reference to questions of environmental control, Kemp & Burtness (1984) have provided an experimental analysis of the influence of different growth rates, mediated through ecological factors, on shell shape. Slow-growing individuals of the marine prosobranch Littorina littorea have thick, attenuate shells, while rapid growers have thin, globose shells, the differences being attributed to limitations on the maximum rate at which calcium carbonate can be secreted. Thus, contrary to Williamson’s statements, there is evidence of variation in shell geometry among prosobranchs both within and between populations. The problem is to distinguish the levels of genetic and environmental control involved. This is difficult enough when studying living molluscs, and even more so when dealing with fossils, yet it has important taxonomic implications. As we are concerned with African freshwater prosobranchs we can begin by referring to cases drawn from that most remarkable of all examples, the radiation in Lake Tanganyika. Kat & Davies (1983) have already noted that the Tanganyikan Meothauma tanganyicense shows phenotypic variation that encompasses the range shown by Bellamya unicolor (to which we refer below). Using outlines traced from photographs in Leloup (1953), Fig. 1 illustrates some of the variation in shell geometry in Edgaria nassa. This is matched by great variation in sculpture, some of which is illustrated in 35 photographs and several drawings by Leloup. Figure 2, also taken from Leloup (1953), shows the shells of a number of individuals of Syrnolopsis lacustris collected at a number of stations in the lake. Clearly like E. nassa, S. lacustris is subject to variation in shell geometry and ornamentation. Other examples from Lake Tanganyika include Anceya giraudi, Paramelania damoni, and P. irridescens, all of which display much variation in both shell form and ornamentation; this is well shown in numerous photographs in Leloup (1953). It is indeed curious that Williamson could cite this work yet ignore that information which challenges the basis of his hypothesis. Nor is the phenomenon confined to Tanganyika. Soapitia dageti provides an African example (Binder, 1962). In passing we would note that while Williamson dismisses as trivial the sudden changes demonstrated by Griineberg (1980, 1981) in various prosobranchs, these are in fact graphic demonstrations of how ‘plastic’ in one particular sense - additional to geometry - the prosobranch shell can sometimes be. As the phenomenon is perhaps not well known, we illustrate in Fig. 3 examples of abrupt changes in the phenotype of certain prosobranchs. Many such changes were described and illustrated by Griineberg, incidentally from among populations that displayed an enormous range of variability in this respect. As to geographic variation, we provided examples in our earlier comments (Fryer et al., 1983). Yet Williamson rejects our statements as “either unconvincing or erroneous” and our references to variation in Bellamya unicolor as “inaccurate”, insisting that B. unicolor is indeed “invariant in basic shell form”, and rejecting our statement that the taxonomy of this species and its relatives “is bedevilled by variation both local and geographical”. It is necessary to answer such comprehensive condemnation. We are surprised that Williamson SPECIATION IN FOSSIL MOLLUSCS 329

Figure 1. Variation in shell geometry and ornamentation in the prosobranch Edgaria nassa in Lake Tanganyika. Outlines traced from photographs in Leloup (1953). so completely failed to understand that we were using B. unicolor as an example of the way in which intraspecific variability could lead taxonomists into recognizing a large number of taxa. The varied opinions of such workers as Mandahl-Barth (1954, 1972), Crowley, Pain & Woodward (1964), Brown (1980), Gray (1980) and Van Damme (1984) reveal both the variability of B. unicolor and its “hardly distinguishable” relative B. capillata (Brown, 1980) and the taxonomic difficulties involved in dealing with such a multiplicity of shell morphologies. Indeed, in a recent review of the freshwater molluscs of N Africa (Van Damme, 1984) B. unicolor is described as “extremely polymorphic” and reference is made to ecological forms that differ in the convexity of the whorls, which may be either smooth or ridged. There is no reason to suppose that our understanding of the taxonomy of this group will not evolve as more refined techniques are brought to bear on the problem. Kat & Davies (1983) also refer to what they call Williamson’s “conception of the narrow phenotypic range of B. unicolor”, with which they disagree, noting that museum collections show a range of variation in this species sufficient to encompass the claimed derivative species in the Turkana deposits. In response, Williamson gives a diagram of principal components analysis of certain data, which at best leaves the matter sub judice, and reiterates his belief that variability 330 G. FRYER ETAL.

Figure 2. Variation in shell geometry and ornamentation in the prosobranch Symalopsis lacustris in Lake Tanganyika. From Leloup (1953). in B. unicolor has “a rather narrow phenotypic range”. On the characters used, his deviant form clusters separately, but in itself this is not proof of distinctness at the species level. Similar comments, arguments and references could be enumerated for Melanoides tuberculata, Cleopatra ferruginea and Pila ovata, but would only reiterate and reinforce the same points. Despite Williamson’s protestations, our statements about the variability of prosobranchs can be substantiated. In view of this variability, the apparent morphological stasis shown for long periods by the fossils is indeed, as we previously stated, “surprising and not easy to explain”. We do not accept, however, that the difficulties largely disappear “when it is appreciated that this stasis is paralleled by the pronounced geographical invariance in fundamental shell morphology exhibited by their modern representatives”, which is not remotely the case. SPECIATION IN FOSSIL MOLLUSCS 331 if f

Figure 3. Abrupt changes of colour patterns in individual shells of three species of marine gastropods (Prosobranchia, Neritacea); specimens in the British Museum (Natural History). Scale = 1 cm. A, Clilhon oualaniensis Lesson, collected Chilwan, Ceylon by Griineberg. B, Nentma turrita Gmelin, various localities. C, Ntritina smithii Wood, Calcutta.

SPECIATION OR VARIATION

Because Williamson’s often-reiterated claim (now modified from one originally even more rigid) that the modern representatives of the Turkana lineages are subject only to “relatively minor variation in shell size, thickness and colour” is demonstrably incorrect, it is difficult to regard unequivocally those morphological excursions that he describes as speciational events. These episodes of “radical phenotypic transformation” occurred at the Suregei and Guomde levels as interruptions during periods of remarkable stasis. They are claimed as documenting speciation events within peripatric isolates. We expressed, and still maintain, reservations about this interpretation. At the Suregei level, members of all 10 lineages studied display deviation from the ancestral form. Williamson believes that the deviants represent new species. We incline to the view that all lineages responded to some common overall environmental change. Boucot (1982) likewise regards such simultaneous speciation events as “a strange coincidence” but thinks the changes are “entirely plausible from the ecophenotypic point of view”. Williamson now argues that no molluscan fauna is known in which every component is represented by ecophenotypic variants. That may be so, but such situations are likely to be rare, though drying lakes or lakes subject to great variations in environmental conditions, such as Lake Turkana, are the sorts of places where they might occur. A demonstration of such a situation would only be possible under strictly controlled experimental conditions. However, single-species populations can illustrate such ecophenotypic shifts and it would seem not unreasonable to 332 G. FRYER E T AL. suggest a similar response among ecological analogues. Thus, three of the four gastropod lineages in the Turkana sequence show the same pattern of diminishing shell globosity and the temporary disappearance of the original globose form. All were epifaunal deposit feeders. The fourth lineage, representing an infaunal deposit feeder, showed the reversed pattern (Kemp & Burtness, 1984). Williamson says that “co-ordinated suites of minor ecophenotypic responses may be elicited in all or most mollusc species” present in extreme environments and mentions shell size and thickness. To him the hallmark of such an environmentally induced response is its “co-ordinated theme” in all lineages present. At the levels in the Turkana deposits where morphological excursions are evident, there is, he says, no such co-ordinated theme. However, one would only anticipate co-ordination among appropriate analogues; otherwise the fact that all lineages of both bivalves and gastropods simultaneously deviate from what was ‘normal’ in shell form is as much of a co-ordinated theme as one could expect in such a diverse assemblage of organisms. Williamson is also puzzled as to why, during this period of ecological rigour and morphological change, no lineage became extinct, and for some reason thinks that this presents us, his critics, with a “particularly vexing problem”. His only reason for so thinking is because he attributes to us his own mistaken conception that the response to “harsh or unusual conditions” is “a reduction in shell size and thickness followed by local extinction in extreme cases”. Where, one asks, does Williamson derive his knowledge of the reactions of molluscs to harsh conditions that leads him to make such suggestions and to deny that they ever react by changes in shell geometry? If the alleged 10 new species were indeed such, it is somewhat curious that, as soon as they came in contact with the parent stock, without exception all became extinct. This is not the pattern seen in other African lakes, such as Victoria and Malawi. Here widespread species coexist with closely related endemics. This is so among the species of Bellamya in Lake Victoria as Williamson himself is at pains to explain, and among those of Melanoides in Lake Malawi. That all 10 allegedly new species should immediately perish on rejoining the ancestral stock is as unlikely as that 10 lineages should simultaneously undergo speciation. That all 10 should simultaneously do both these things is even more improbable, indeed implausible in the light of current knowledge. Hence our unease at their transitory nature about which Williamson complains. Williamson also believes that an obstacle to explaining the Suregei level novelties as ecophenotypes is the presence there of “highly variable populations morphologically and stratigraphically intermediate” between them and their ancestors. He thinks that no such variable populations are known from any modern faunas - and says we are “clearly aware” of this! - and that whole populations usually respond in the same way to environmental influences. A glance at Figs 1 & 2 is sufficient to dispel any such misconception. We are also aware of the subtle patchiness of many environments, giving rise to different behavioural and morphological variations of animals over very short distances - sometimes a matter of a few metres. A well-studied marine prosobranch that displays this phenomenon is Nucella lapillus (Cooke, 1895; Berry, 1977; (both with illustrations) Berry & Crothers, 1968). This phenomenon is accentuated in species such as these freshwater prosobranchs with no dispersal phase. Any SPECIATION IN FOSSIL MOLLUSCS 333

taphonic assemblage from such populations could exhibit a diverse array of morphologies. A recent study on the marine prosobranch Nucella emarginata is also very relevant here as it shows how the already known variability of this species is controlled by both genetic and environmental factors. Palmer (1985) has now demonstrated that a major component of the usually conspicuous spiral sculpture of this species is inherited in a Mendelian manner, sculpture being dominant to lack of it. He also showed that the phenotypic effects of the gene or genes controlling sculpture can be modified by environmental conditions. Palmer notes that these results draw attention to the difficulty of inferring speciation from changes in shell morphology and that “in particular, they indicate that certain ‘quantum’ changes in lineages of fossil gastropods could result from gene frequency changes of one or a few loci and hence need not reflect a ‘genetic revolution’ associated with speciation”. Referring to the Lake Turkana fossils, Palmer notes that Williamson’s findings could be explained by such changes in gene frequency, by rapid change in phenotype from one fitness peak to another, or by simple ecophenotypic changes. The claim that the fossils reveal speciation is deemed “tenuous at best”. In discussing Melanoides tuberculata, assumed to be parthenogenetic, we suggested, as did Mayr (1982), that many clones were likely to be involved. Williamson complains that we offer no evidence for this assertion and accuses us of ignorance on the subject of interclonal competition. Work on Daphnia shows that many clones often coexist. Carvalho (1985) has shown that a population of D. magna in a very small lake “probably consisted of many hundreds of clones throughout the year” and Lynch (1984) notes that a pond population of D. pulex consisted of three clonal groups of which one was entirely parthenogenetic, the other two cyclically so, and “probably consist of thousands of clones during most periods of clonal reproduction”. These cases admittedly include bouts of sexual reproduction and Lynch demonstrates severe competition, but the persistence of completely asexual clones in the face of competition from a minimum of 105 new clones hatching each spring from resting eggs makes sweeping assertions about competitive elimination dangerous. Furthermore, interclonal competition can be reduced by temporal variation in environmental conditions, different clones being favoured at different times, and Hebert (1982) points out that experiments have shown that clones with small genetic distances are less likely to exclude each other than are less genetically similar clones, because fitness differences will be small. On this issue the Turkana material can never produce evidence - a limitation of fossil m aterial. Experim ents w ith living M . tuberculata m ay do so. Furthermore, the entire argument may be academic in this case. Hitherto believed to be an obligate parthenogen, the rare males seen in certain populations being sterile, this species has recently been shown to consist of both parthenogenetic and bisexual populations, at least in Israel and the Sinai region (Livshits & Fishelson, 1983; Livshits, Fishelson & Wise, 1984).

LIVING FISHES, FOSSIL MOLLUSCS AND THE DEMONSTRATION OF SPECIATION It is disconcerting to find several misquotations and misinterpretations in the section of Williamson’s reply dealing with the question of cichlid fishes,

18 334 G. FRYER ETAL. punctuated equilibrium and speciation. These detract from and confuse the main thrust of the discussion. Thus, we did not attempt to dispute the punctuated equilibrium model, and indeed have suggested that cichlid fishes provide examples of such an evolutionary pattern (Greenwood, 1981, 1984). Our major disagreement with Williamson here, however, is with the cavalier manner in which he dismissed our claim that extant cichlid fishes present a far better example of rapid speciation in African lakes than does the Turkana sequence of fossil molluscs. There are many situations among African cichlids in which rapid speciation can be demonstrated in an almost diagrammatic manner. The isolation and subsequent evolution of endemic species in Lake Nabugabo is one example. Others concern fishes in Lakes Malawi and Victoria that have undergone speciation that, as shown by electrophoresis (Kornfield, 1978; Sage, Loiselle, Basasibwaki & Wilson, 1984), must have been extremely rapid. These taxa now form complex assemblages of sibling species that apparently cannot be separated on orthodox morphological or morphometric criteria. However, the species differ strikingly in male coloration, territorial behaviour and intralacustrine distribution, sometimes have demonstrable ecological preferences, and frequently coexist without interbreeding. We are also amazed that Williamson was provoked to say “The fact of the matter is that groups with no fossil record - such as the cichlid fishes have simply not provided us with detailed and unambivalent information about the fine-structure of events during speciation”. The previous paragraph partially refutes this. In making further points, we stress that this is not an argument attempting to show the superiority of one discipline over another. Speciation is a historical event and fossils can in theory preserve steps in the process - but so in some cases can living animals. Furthermore, as Ruse (1984) has remarked, while the fossil record gives invaluable evidence with regard to the path of evolution, it is only of secondary importance when one is concerned with the mechanisms. In the revelation of evolutionary pattern and process the strengths of palaeontology and biology are very different. A major limitation of fossils is that they can preserve only the morphological consequences of speciation. However, there may not be any morphological consequences, as cichlid fishes and other animals clearly show (e.g. Marsh, Ribbink & Marsh, 1981; Ribbink, Marsh, Marsh, Ribbink & Sharp, 1983; Ribbink, Marsh, Marsh & Sharp, 1983). There is also the problem of deciding from morphology alone what constitutes speciation. This can be particularly acute in cases involving sibling species or polymorphism. Some cichlid fishes of the genus Cichlasoma display remarkable polymorphism involving such hard parts as the pharyngeal bones. That this was indeed polymorphism was only resolved by observations on ecology and breeding behaviour combined with electrophoretic studies (Kornfield, Smith & Gagnon, 1982). African cichlitl fishes in fact present some of the clearest evidence bearing on events taking place during speciation (e.g. Fryer & lies, 1972; Marsh et al., 1981). Rather than reiterate reported facts we would note that, as well as soft-part anatomy, students of speciation in cichlid fishes (and other living organisms) have at their disposal a wide array of techniques and observational possibilities few of which are available to the palaeontologist. These include karyological, electrophoretic, chromatographic and serological techniques, and the study of breeding behaviour, breeding seasons, habits, coloration and subtle differences in ecology and local distribution. Most SPECIATION IN FOSSIL MOLLUSCS 335 important of all, they often have the potential to investigate whether interbreeding occurs in nature within sympatric populations.

CONCLUSIONS Rather than attempting to summarize our disagreements with Williamson we would refer to the conclusion of our previous paper where we draw attention to the mutually illuminating possibilities provided by the fossil and extant assemblages of organisms in African lakes. Opinions constantly change in the light of new evidence, and by attempting to defend every statement he has made, even when these appear untenable, we feel that Williamson is more likely to hinder than to assist the process of understanding.

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NOTE ADDED IN PROOF

Recent studies of Bellamya by Dr P. Kat (National Museums of Kenya) have illuminated some interesting patterns of speciation in freshwater prosobranchs (pers. comm.). Considerable variation exists at both the chromosomal and molecular levels in species sampled from a wide range of habitats in eastern and central Africa. Diploid numbers can vary between 10, 12, 18, 22 and 24 and the form of the chromosomes may be predominantly meta- or acrocentric in some populations. Quoting Kat: “more genetic change might have taken place during the 97% of his (Williamson’s) shell shape stasis than during the 3% time of shell shape change”. Indeed, in one figure of Williamson’s paper specimens with, at least, 10, 18 and 22 diploid chromosome numbers have been grouped into a single species. These preliminary results add another dimension to the whole problem of interpreting shell shape in terms of speciation events.