Biological Journal of the Linnean SocieQ ( 1983),20: 195-205
Punctuated equilibria, morphological
stasis and the palaeontological
documentation of speciation: a biological
appraisal of a case history in an African lake
G. FRYER,
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 f o r publicalion December I982
The present-day faunas of the great African lakes present some of the world’s best examples of
‘explosive speciation’. Lakes Victoria and Malawi each probably have several hundred endemic
species of cichlid fishes. Much can be inferred about the evolution of these fishes from morphology,
behaviour and intra-lacustrine distribution and from the fact that they include taxa ranging from
local races, through sibling species, to forms that display extensive differentiation. The time taken to
acquire specific distinctness can sometimes be accurately defined, but fossil lineages are unknown. A
recent study of a fossil sequence of molluscs in the Turkana basin throws new light on the history of
African lake faunas. It also claims to have resolved events during speciation. While critical analysis
based on our knowledge of living molluscs in this area fails to substantiate this claim, the fossil
molluscs complement information provided by the biology of extant fishes and invertebrates and
emphasize the importance of these lakes in the study of evolution in living and extinct populations.
KEY WORDS:-Speciation
- morphological stasis
molluscs - cichlid fishes - African lakes.
-
variation
-
punctuated equilibria
fossil
CONTENTS
The problem . . . . . . . . . . .
Phenotypic variation in freshwater molluscs.
. . .
Speciation or ecophynotypic change? . . . . .
Punctuation and stasis-the limitations of fossil evidence
African lakes and evolutionary biology . . . . .
References.
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203
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T H E PROBLEM
A continuing debate among students of evolution is whether change has been
gradual, as frequently assumed, or episodic as postulated in the ‘punctuated
equilibrium’ model of Eldredge & Gould (1972) and Gould & Eldredge (1977).
+
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195
0 1983 The Linnean Society of London
196
G . FRYER E T AL.
One of the most interesting examples described in support of the punctuation
model is the analysis by Williamson (1981a) of a sequence of late Caenozoic
freshwater molluscan lineages in the Turkana basin in Northern Kenya. This
claims to present a fine-scale palaeontological resolution of events during
speciation, and to demonstrate long-term morphological stasis. Although based
only on fossils and restricted to a single group of organisms, the study is of great
relevance to the investigation of the evolution of present-day African lake
faunas.
These extant lake faunas illustrate many evolutionary phenomena, including
some of the world’s most dramatic examples of so called ‘explosive’ speciation.
For example, Lakes Victoria and Malawi each have over 200 endemic species of
cichlid fishes. Much can be inferred about the evolution of these fishes from their
morphology, behaviour and intralacustrine distribution, and the fact that they
embrace taxa ranging from local races, through sibling species, to forms that
display a high degree of morphological differentiation. In some cases even the
time taken to acquire specific distinctness can be identified within narrow limits
(Greenwood, 196513) though fossil lineages are unknown. It might therefore be
anticipated that the discovery of a well-documented fossil sequence of Mollusca,
another group of animals showing considerable radiation in African lakes,
would throw light on the history of these lacustrine faunas.
Williamson’s paper has already stimulated considerable interest and criticism
Uones, 1981; Anon et al., 1982). These comments, however, are largely
theoretical and pay scant attention to the animals themselves, many of which
still exist in African lakes; and no comparisons are made between events in the
fossil record and situations that exist today. Here, we discuss certain attributes of
the organisms concerned, review some other groups of animals in the African
lakes, and consider, in the context of modern faunas, some of the observations
and conclusions derived from Williamson’s study of fossils.
PHENOTYPIC VARIATION IN FRESHWATER MOLLUSCS
The Turkana fossil sequence shows that for long periods the species involved
display morphological stasis in shell form, interspersed with shorter periods in
which well-marked shifts in phenotype occur simultaneously in several
populations. Williamson stresses the phenotypic stasis in both sexual and asexual
gastropods and claims that it ‘% paralleled by the geographical stability of
phenotype exhibited by their widely distributed modern representatives; shell
form in the lineages studied is normally highly ‘heritable’ (the extreme
ecophenotypic variability of freshwater Basommotophora is not typical of the
gastropods studied here, most of which are prosobranch species characterized by
narrow phenotypic ranges in modern faunas)”. He also stresses that “the long
term temporal stasis in morphology exhibited by these lineages and their current
morphological stability in a diverse range of modern environments, preclude the
possibility that such dramatic phenotype shifts are in any sense ‘non-genetic’ or
‘ecophenotypic’ ”.
The absence of a full taxonomic account of the Turkana material places a
major constraint on a detailed discussion of Williamson’s analysis. Nevertheless,
his claims seem scarcely in keeping with the facts. Warnings given in an
introduction (Cox el al., 1969, pp. N413-N414) to the superfamily Unionacea in
EVOLUTIONARY PATTERNS IN AFRICAN LAKES
197
the Treatise of Invertebrate Paleontolou are pertinent here, for Williamson includes
several members of this group in an analysis of what he claims are speciation
events. The remarks stress that LLvariationsthat reflect ecological factors must
not be overlooked in the study of the classification of Unionacea, for otherwise
erroneous conclusions as to the taxonomic significance of divergent or
convergent shell characters are invited. Owing to the ecological plasticity and
the rapidity and wide range of dispersal of these freshwater clams by fish-borne
larvae, a single generation may produce offspring that on reaching maturity
differ notably from parent forms. This is strikingly illustrated by comparing the
completely sculptured shells of unionids in eastern African lakes with
taxonomically equivalent smooth shells in streams that empty into these lakes.”
Variation within a lake is also known, for example, in both species of Caelatura
listed by Williamson (1981a) among the Turkana fossils (see Mandahl-Barth,
1954). Marked variability, not just in sculpture but in shell form, is indeed
known in African, and other, bivalves. This is clearly illustrated in the revision
of bivalves from Lake Tanganyika by Leloup ( 1950).
Likewise, in an introduction to a revision of the Australian freshwater mussels,
McMichael & Hiscock (1958) review ecophenotypic effects in relation to species
concepts, and note that whole populations are frequently affected by
environmental conditions that impose phenotypic changes on shell morphology.
In a still earlier review, Eagar (1948), discusses variation in shell form among
both fossil and living freshwater bivalves in relation to ecological conditions.
Similar reservations must be expressed with regard to gastropods.
Information on variation in African snails is uneven as it tends to reflect the
intensity of investigation. Hence extensive data on ecophenotypic variation
exists for the medically important groups of the Basommatophora: these are
supported by breeding experiments. For the relatively unimportant
prosobranchs, which are prominent elements in the Turkana formations, the
data are more limited. It is perhaps this disparity which led to Williamson’s
comment that the extreme ecophenotypic variability of freshwater
Basommatophora “is not typical of the gastropods studied here, most of which
are prosobranch species”.
One of the Turkana species considered by Williamson is Bellamaya unicolor, a
taxon which hardly displays “morphological stability in a diverse series of
modern environments”. O n the contrary, the taxonomy of this species and its
relatives is bedevilled by variation, both local and geographical, a situation
reflected in the recent literature on the group. I n Lake Victoria alone MandahlBarth (1954) recognizes nine named varieties on the basis of shell form. These
(which he treats as subspecies) differ in shell size, shape, ornamentation and
colour. Brown (1980) suggests, however, that this picture must be modified as
some forms should be raised to specific status and others transferred to closely
related taxa. Nevertheless, even as currently conceived, B. unicolor still displays
considerable variation.
Closely related to B. unicolor is B. capillata, a species whose shell, “is hardly
distinguishable from that of B. unicolor if the variety of local forms assigned to
each species is considered” (Brown, 1980). Indeed Brown only tentatively
accepts the specific distinction on the basis of the statement by Mandahl-Barth
(1973) that B . capillata differs from B. unicolor in having fewer and larger
embryos, a feature unlikely to be recorded in fossils. The chequered taxonomic
I98
G. FRYER E l A L
history of this group demonstrates the difficulties that confront even the student
of the living animals and shows the close association between the assessment of
variability and differing species concepts.
Species within the geographically widespread genus Cleopatra provide further
examples of great variability in shell morphology. Various forms of C. bulinoides
were once recognized as distinct species, and there is now even some doubt
about the distinctness of C. ferruginea (Brown, 1980), one of the taxa reported
from Turkana. Similar problems are presented by Pila ovata, which was also
studied by Williamson. This is variable in shape, size, thickness and colour of
the shell according to habitat, and several forms have been described even
within one lake (e.g. Leloup, 1953; Mandahl-Barth, 1954).
The central problem is to determine the degree to which variation is under
genetic control and how relevant it is as an indicator of speciation. Studies on
Oncomelania hupensis, a small freshwater prosobranch snail from Asia, suggest
that, at least in some taxa, variation in shell sculpture is associated with
differentiation into forms. These features appear sometimes to be under simple
Mendelian control although ecological features may also be involved (Davis &
Ruff, 1973). This contrasts with the examples of ecophenotypic variation in
colour patterns occurring in another prosobranch, Theodoxusjuviatilis (Neumann,
1959a, b). Here abrupt changes from one pattern to another, and back again,
can be induced by manipulating the environment. Similarly in natural
populations of the marine Clithon oualaniensis and species of the genus Umbonium
environmental factors may be involved, as the phenotype can change abruptly
during the lifetime of a single individual (Gruneberg, 1976, 1980, 1981).
Notwithstanding such information a n understanding of variation in natural
populations is hampered by the absence of breeding experiments under
controlled conditions. These are often difficult to perform and to interpret. For
example, in the basommatophoran Lymnaea stagnalis, exposure to a particular
environment at the egg stage may determine shell shape throughout ontogeny
(Roszkowski, 1914; Arthur, 1973). This susceptibility has been used in the study
of morphogenesis (Raven, 1966), where traces of certain chemicals in the
environment produce major distortions of the shell. Such factors may well have
operated in fluctuating environments such as prevailed during the history of the
Turkana Basin (Abell, 1982).
Williamson attaches particular importance to the asexually reproducing
Melanoides tuberculata. This is another species that is variable in shell form. For
example, Mandahl-Barth ( 1954) illustrates two extreme forms from Lake
Victoria, and there are striking differences in maximum size, and sometimes in
shell thickness, between populations at different localities in east and central
Africa, even where they are sympatric with endemic species (Mandahl-Barth,
1972). In both instances the relative contributions of environment and heredity
are uncertain. Thus shifts in the phenotype of fossil M . tuberculata populations at
certain horizons in the Turkana formations could imply phyletic change, as
suggested by Williamson. Alternatively they could indicate merely differing
reactions by the same genotype to a variety of environments-in
spite of his
view that ecophenotypic change played virtually no part in the history of the
populations. An experimental approach to this problem is desirable, considering
the unusual environmental conditions in Lake Turkana today (Talling &
Talling, 1965).
EVOLUTIONARY PATTERNS IN AFRICAN LAKES
I99
SPECIATION OR ECOPHENOTYPIC CHANGE
The evidence for speciation in the Turkana fossil molluscan lineages appears
to be susceptible to other explanations. The fact that “major phenotypic
transformations occur simultaneously in all lineages at the Suregei tuff level”
suggests ecophenotypic shifts rather than genotypic changes associated with
speciation. This conclusion is reinforced by the transitory nature of these taxa.
We consider that simultaneous change in 10 species belonging to widely
divergent taxa is more likely to be a phenotypic response to environmental
stress, such as a change in alkalinity or salinity, than 10 simultaneous speciation
events in different lineages. Williamson’s reply (in Anon et al., 1982) to a similar
criticism is that “The principal stem lineages in the Turkana Basin sequence are
still extant and widely distributed in Africa, but even the most extreme modern
environments in which these lineages occur at present produce a simple
dwarfing of characteristic morphology (or in extremis, extinction of local
populations), they never produce the striking reorganization of phenotype
documented in the Turkana basin sequence”. This is not so. There is wide
variation, both within and between the lakes, for many of the species that
Williamson claims never produce the sort of phenotypic reorganization
documented in the Turkana sequence. Similarly his statement that “the
magnitude of the changes documented in both the bivalves and gastropods is
generally far greater than that observed in the ecophenotypic transformations of
even the most plastic of modern African freshwater molluscs” appears to be
untrue and ignores published evidence (see above).
If environmental influences are important, the morphological changes in the
obligatory asexual Melanoides tuberculata cease to present a genetic problem as
ecophenotypic modification of shell form does not depend on sex, and the
problem raised by Jones (1981) of an obligate parthenogen apparently evolving
as rapidly as its sexual relatives calls for no solution as it is illusory. I n addition,
Mayr (in Anon et al., 1982) notes that many clones of Melanoides are likely to
have been involved and asks how all of them experienced a parallel history of
equivalent genetic changes. Williamson suggests that only one or a few clones
underwent these changes and that they outcompeted conspecific clones. This is
not very convincing: it is more likely that many clones were involved. If so, their
concordant change suggests that these were merely environmentally imposed
modifications.
The increase in phenotypic variance observed in certain species at the Suregei
tuff level is also not surprising if the observed transformations were
environmentally imposed. Such changes might be induced epigenetically, and
different genotypes could differ in the extent of the interactions and in the speed
of reaction to environmental change. This might give an impression of a gradual
directional change. Certainly the populations would have been subjected to
variations-in salinity or alkalinity as the habitat contracted and expanded
during dry or rainy periods. The oxygen isotope record, using mollusc shells as
the source of measurement (Abell, 1982), indicates that the environment here
was indeed changing rapidly.
Williamson (1981a,b) lays great stress on what he interprets as developmental
instability accompanying ‘speciation’ among the Turkana fossil molluscs. He
believes that morphological stasis is primarily a result of developmental
200
G. FRYER E l d L
homeostasis (sensu Mayr, 1963) and that by definition speciation must “involve
the dismantling of homeostatic mechanisms pre-existing in the parental stock”.
Such dismantling would presumably be associated at some stage with increased
morphological variability prior to the re-establishment of a new morph. It is
interesting that increased variation is also linked with populations expanding in
response to favourable environmental conditions (Ford & Ford, 1930; Ford,
1945). For the fossil molluscs from the Turkana formations these changes in the
environment and the increasing population size could be consequent upon
higher rainfall.
The abrupt return to ancestral morphology immediately above the Suregei
tuff and Guomde levels could be explained either by an invasion of ancestral
forms of superior fitness (Williamson, in Anon et al., 1982), or by a reversion of
the phenotype to the ancestral condition on removal of an environmental stress.
We cannot agree that events at the Suregei tuff and Guomde levels “provide, for
the first time details of allopatric speciation during the ‘punctuation’ of
cladogenesis” or that “they allow an unprecedented resolution of the fine
structure of events during speciation”.
Evidence for the development of genetically distinct forms is more convincing
in the lower member of the Koobi Fora formation, where novel morphs co-exist
with their parent forms; although this does not constitute proof of speciation,
since particular segments of a population could react to stimuli in different
ways. This co-existence throws further doubt on the claim that other
morphological excursions-where
the ancestral form disappears-represent
speciation events.
It is also necessary to treat with some caution the assumption of phenotypic
stability in certain species involved in the Turkana fossil sequences. The
apparent morphological stasis exhibited over long periods by species that are not
renowned for their phenotypic stability in extant populations is surprising and
not easy to explain. Here again, we are constrained by the lack of a detailed
taxonomic account of the fossils.
PUNCTUATION AND STASIS-THE LIMITATIONS OF FOSSIL EVIDENCE
To account for speciation amongst the Turkana fossil mollusc fauna
Williamson (1981a) invokes the allopatric speciation model. The same model
has been used to explain both the origin of the greater part of the species flock of
haplochromine cichlid fishes in Lake Victoria (Fryer & Iles, 1972; Greenwood,
1974) and their relationship to the Lake Nabugabo species from which they
were isolated about 4000 years ago (Greenwood, 1965b; Fryer & Iles, 1972).
As is obvious, we are sceptical as to whether the morphological changes
recorded for the molluscs from the Turkana formations can be accepted as
evidence of speciation. In our view, a far better example of rapid speciation
(punctuation) and its associated morphological differentiation (or lack of it) is
provided by the species of haplochromine fishes in Lake Victoria. These fishes
illustrate the difficulties that an investigator would encounter if they were
known only from fossil remains. Under these conditions it would be impossible
to recognize many of the species simply on the basis of their body form, fin-ray
numbers, scale counts or most osteological and dental characters. In life,
however, the species differ markedly in their behaviour, physiology, ecology and
EVOLUTIONARY PATTERNS IN AFRICAN LAKES
20 1
breeding coloration. For example, the Nabugabo cichlids are most readily
distinguished from their relatives in Lake Victoria by difference in male
breeding coloration, a species-specific feature important in these fishes since it is
involved in species recognition. Furthermore, the co-existence in Lake Victoria
of numerous, closely-related but non-interbreeding taxa, adds credence to their
status as true species, a status which might be queried if it was based only on
anatomical and meristic features. The nature of the species in palaeontology is a
continuing topic for debate; see for example, Forey (1982: 150-157) and
Joysey (1972).
Similar problems of differentiation are encountered in the study of living and
fossil molluscs, and it is important to appreciate the significance which is
attached to the ‘soft parts’ and other attributes of the living animals. The
significance of such features is apparent a t all taxonomic levels and is well
illustrated by two families of bivalves. Mutelid and unionid molluscs represent
ancient lineages that have very similar shell forms, so similar indeed that until
recently an entire Australian fauna of large freshwater bivalves was assigned to
the Mutelidae when in fact it belonged to the Unionidae, an error at family
level. Within their relatively unchanging shells these two groups have diverged
in remarkable ways, having acquired different life cycles and very different
larval forms. I t was the discovery of the life cycles of mutelids (Fryer, 1959b,
1961; Bonetto & Ezcurra, 1962a, b) that led to a re-investigation of the
Australian fauna and the demonstration of its true affinities (McMichael, 1967).
These life cycles, involving minute, short-lived larvae and parasitic phases, are
something on which the fossil record is likely to remain silent. Purely fossil
evidence on the history of these lineages would give a misleading impression of
stasis in a group which has in fact undergone fundamental evolutionary change.
Cichlid fishes provide information relevant to the problem of ecophenotypic
change. A particularly apt case is provided by the pharyngeal bones and
dentition of Astatoreochromis alluaudi. In Lake Victoria this species feeds largely
on hard-shelled molluscs, especially Melanoides tuberculata, which it crushes
between the molariform teeth of its robust upper and lower pharyngeal bones
(Greenwood, 1959). However, in other lakes, where the snails are thin-shelled
(or if the fishes are reared on soft foods) these bones are weakly developed and
there is a marked reduction in the size and number of molariform teeth
(Greenwood, 1965a). Fossils from populations eating thick- and thin-shelled
snails would probably be assigned to different species by the unsuspecting
palaeontologist. Pharyngeal bones and dentition often provide useful taxonomic
characters, and interspecific differences such as these would be, to borrow
Williamson’s phrase, “outside the narrow phenotypic range’’ of most species.
The co-existence of many closely related species among lacustrine cichlids
clearly illustrates the problem of species recognition. I n Lake Tanganyika
Tropheus moorii is split into numerous isolated populations along the shore
(Marlier, 1959; Matthes, 1962; summary in Fryer & Iles, 1972). Many of these
are distinguished by distinctive coloration and may represent subspecies or even
species; speciation has been achieved in one area where 1.duboisi co-exists with
T. moorii. If fossilized, these taxa could not be told apart, but in life they differ in
their ecology and behaviour as well as in certain juvenile attributes, and co-exist
without interbreeding.
The two sibling species of Labeotropheus in Lake Malawi (Fryer, 1956, 1959a)
202
G. FRYER E T AL.
are so alike that they were thought to be conspecific by Balon (1977), but recent
work shows that they differ in male coloration, in depth preferences and in their
ability to equilibrate to pressures at different depths (Ribbink et al., in press).
Likewise the genus Petrotilapia of the same lake, once thought to be monotypic,
now proves to be a complex of at least 17 sibling species (Marsh, Ribbink &
Marsh, 1981 and unpubl. data) which cannot be separated with confidence on
the basis of morphometric features or on any differences in dentition, but which
differ in colour and territorial behaviour. Their distinctness is attested to by the
frequent syntopic co-existence of two or more species.
Williamson claims that the Turkana fossil sequences conform to the
punctuated equilibrium model and that “no gradualistic morphological trends
occur in any lineage”. This does not agree with his statement that a t certain
levels there are populations of Bellamya unicolor “morphologically intermediate
between this unusual form” and the parent type. He also lists other species in
which there are “populations intermediate between typical representatives of
those lineages, and their distinctive derivatives at the Suregei tuff level”. I n the
Koobi Fora sequence, the “novel morphs” of Melanoides tuberculata are also said
to have arisen “via intermediate forms”.
The extant cichlid fishes of the African lakes demonstrate the difficulties
inherent in the more rigid punctuationist and gradualist views. The enormous
and morphologically diverse species flocks of these fishes have evolved rapidly:
specific distinctness has been acquired by the Nabugabo endemics in about 4000
years. Moreover, for Lake Malawi cichlids it is suggested on the basis of
electrophoretic studies that “extremely rapid speciation is supported by the low
degree of genetic differentiation amongst these species” (Kornfield, 1978).
At present the evidence indicates that these various lacustrine cichlid faunas
were derived from a few generalized species in a matter of $ to, at most 3 My
(see Fryer & Iles, 1972; Greenwood, 1981). Since they are highly speciose, and
show a wide range of morphological divergence their origins can be regarded as
punctuational (sensu Eldredge & Gould, 1972). At the same time, however,
many of the co-existing species are living representatives of stages in the
development of various morphological specializations. In that sense the picture
appears to be one of gradualism, but it is important to realize that the various
stages, in these apparently gradual changes, are represented by separate species.
Hence, the introduction of the term ‘cladistic gradualism’ to describe this
phenomenon (Greenwood, 1981). Indeed, as evidence of a punctuational phase in
evolution, the sympatric species of a cichlid flock seem to provide a better, and
less equivocal, example than do the fossil molluscs of Lake Turkana.
Williamson’s findings present interesting examples of apparent stasis (in
changing environments?) that would repay further analysis as they involve
species which today are not renowned for such stability. Examples of long-term
stasis among African freshwater fishes need not be considered here, but a
dramatic example of what was perhaps short-term stasis in an insect, followed
by an outburst of variation and then a return to stasis, is relevant to the
situation displayed by the Turkana fossil molluscs. This concerns a population of
the marsh fritillary butterfly (Euphydryas aurinia) studied over a period of 55
years (Ford & Ford, 1930). To quote Ford (1945), “the amount of variation was
small during the first period of abundance and while the species was becoming
scarce, and it may be said that a constant form existed at this time, from which
EVOLUTIONARY PATTERNS I N AFRICAN LAKES
203
departures were infrequent. When numbers rapidly increased, an extraordinary
outburst of variation took place so that hardly two specimens were alike, while
extreme departures from the normal form alike in colour, pattern and shape,
were common. A high proportion of these were deformed in various ways, and
some could hardly fly. When the rapid increase had ceased, such abnormalities
practically disappeared and the colony settled down once more to a
comparatively uniform type. This, however, was recognizably different from the
one found during the first period of abundance.” Clearly, in this example
evolutionary changes occurred, but not speciation.
AFRICAN LAKES AND EVOLUTIONARY BIOLOGY
Although we are unable to agree with much of what Williamson claims, we
believe that his findings throw into relief some of the intriguing problems
presented by the faunas of the African lakes. We would also draw attention to
the mutually illuminating possibilities of studies such as those on the fossil
molluscs of the Turkana Basin, investigations on palaeoclimates to which they
contribute (e.g. Abell, 1982))and of studies on the biology of extant lake faunas.
Comparison of past events revealed by the fossil record and of the situation in
the actively evolving cichlid fishes may, for example, help to resolve the
question of whether, as Williamson contends, “speciation is a qualitatively
different phenomenon from gradual intraspecific microevolutionary change”,
or, as the fishes seem to indicate, this is often not the case. T h e possibility of
approaching such questions from different standpoints, our gradually increasing
understanding of the histories of the African lakes, and their great faunal
diversity, together emphasize their outstanding significance as sites where
evolutionary phenomena can be studied both historically and at the present
day.
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