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Biological Journal of the Linnean Socieg (1991), 43: 263-272. With 7 figures
What about non-adaptive radiation?
E. GITTENBERGER
Systematic <oology Section, Leiden University, c/o Rijksmuseum van Natuurlijke Historie,
P.O. Box 9517, JVL 2300 R A Leiden, The Netherlands
Received 23 February 1988, accepted f o r publication 21 March 1990
The use of the epithet ‘adaptive’ in the popular denotation ‘adaptive radiation’ suggests that
radiation as such does not imply adaptation. Without trying to define radiation more sharply than is
usually done in textbooks, emphasis is given to what might be called non-adaptive radiation, a kind
of diversification not accompanied by adaptation into various significantly different niches and,
therefore, resulting in a group of allopatric species which are isolated because of competitive
interactions.
KEY WORDS:-Radiation - adaptive radiation
adaptation - speciation - Albinaria.
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non-adaptive radiation
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diversification
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CONTENTS
Introduction . . . . . . .
Adaptive versus non-adaptive radiation
Sympatric versus allopatric diversity .
Exemplifying Albinaria . . . . .
Individuality of various taxa . . .
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Conclusion
Acknowledgements
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References
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27 1
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27 1
INTRODUCTION
Radiation is a vaguely defined, but popular term in evolutionary biology,
where it is most frequently used in combination with the epithet adaptive.
If radiation is supposed to imply ecological specialization, thus adaptation,
‘adaptive radiation’ becomes a tautology. T o avoid this consequence, radiation
as such should be defined purely taxonomically, as the evolution of a relatively
large, monophyletic group of species or higher taxa.
Because monophyletic groups exist at various levels and in countless numbers,
there are an indefinite number of intermediate situations between a single
speciation event and a radiation. It is impossible, therefore, to define a
borderline between what Davis (1981: 1) called “macroradiation, which
encompasses higher taxa, such as the Mammalia” and a “first order radiation”,
which “consists of a single genus”. The concepts of high taxon and genus are
themselves too ill defined. This causes a terminological vagueness which is
beyond the scope of the present paper.
00244066/91/080263
+ 10 $03.00/0
263
0 1991 The Linnean
Society of London
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E. GITTENBERGER
ADAPTIVE VERSUS NON-ADAPTIVE RADIATION
In most textbooks only adaptive radiation is mentioned although the use of an
epithet suggests that there might be another kind of radiation. Logically,
adaptation should be relevant in adaptive radiation. In that case, the speciation
events will result in species occupying different niches, because they specialized
in various directions. In principle such species can live in the same places. The
large numbers of sympatric cichlid species in certain African lakes are among the
most illustrative examples of adaptive radiation (Fryer & Iles, 1972).
As another consequence of the preceding way of reasoning, non-adaptive
radiation should denote evolutionary diversification from a single clade, not
accompanied by relevant niche differentiation. Because of competitive
interactions, the various species resulting from this process would, in principle,
not be able to be sympatric (Gause’s rule). Their ranges would be largely
allopatric and (very) small if the radiation had occurred in a relatively small
area. There could be mosaic distributions, with populations of closely related
species alternating. Patterns like this are not uncommon in nature. The question
is whether such patterns result from non-adaptive radiation.
SYMPATRIC VERSUS ALLOPATRIC DIVERSITY
Solem ( 1984) has distinguished between sympatric and allopatric diversity.
This is an important distinction and could be a relevant step towards the
acceptance of the concepts of both adaptive and non-adaptive radiation. Solem
(1984: 13) mentions “an amazing radiation of camaenid land snails”
(Pulmonata: Camaenidae) , with populations of different species having “clearly
delineated allopatric ranges”. It could be hypothesized that the morphological
and physiological changes in each of the forms at speciation have caused an
increased fitness to the environments into which they have adaptively speciated.
The habitats look very similar to the human eye, but might not be so for the
snails. The allopatric ranges might not be indicative of competitive interactions,
because of a lack of niche specialization, but could be simply a consequence of
the isolation of the various species because of their low mobility. However,
repudiating dogmatism, it can be hypothesized equally well that adaptation has
been irrelevant in initiating the radiation of the camaenid snails reported upon
by Solem. The various species might still occupy very similar niches both in their
closely resembling areas of origin and in their present occurrence. As a
consequence, competitive interactions might forbid their sympatric occurrence.
In snails, species-specific inhibitory substances in the mucus may aid in keeping
the species apart (Smallridge & Kirby, 1988); however, the significance of this
mechanism in nature is still largely unknown. If a low mobility of the various
species makes interactions very unlikely, there is still no obvious reason to prefer
the view that the allopatric diversity has originated by specializations in various
directions. However, in a supposed subsequent phase, brought about by future
climatic and associated habitat changes for example, which resulted in more
intense secondary contacts, there might be adaptations to (more narrow)
different niches and coexistence, thus more sympatric diversity. Then the
radiation would enter a truly adaptive phase.
NON-ADAPTIVE RADIATION
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EXEMPLIFYING ALBINARIA
The genus Albinaria (Pulmonata: Clausiliidae) contains over 75 species and
many more subspecies (Nordsieck, 1979; personal observations). Only rarely do
more than two Albinaria species live in the same place and often only a single
species is found at a site. There is a bewildering variation in shell form and
sculpture. All the taxa are concentrated in Greece and parts of the adjoining
countries. The species occur in limestone areas which are relatively dry and
warm most of the year. They cannot be considered local forms of only a few
biological (reproductively isolated) species, because they are well characterized
by both conchological and anatomical characters. In comparison with the
extreme intrageneric diversity, populations of Albinaria are usually surprisingly
uniform. Despite this, the systematics of the genus is not clear. This is because of
the large number of (sub)species existing in nature and the vast amount of
literature on them, containing errors and misleading notes, partly resulting from
incomplete original descriptions.
There is some ecological differentiation between so-called ground dwellers and
inhabitants of rock-faces. However, field observations by the present author and
co-workers (E. C. Flach, Th. C. M. Kernperman, N. Reitsma &
M. Schilthuizen) make it clear that a spatial segregation of individuals
belonging to different Albinaria species may depend upon the state of activity of
the animals. Specimens of a species sheltering at ground level during dry periods,
may be actively crawling around on a variety of substrates, including open rockfaces, when the temporal humidity allows it. The more strict inhabitants of rockfaces do not shelter from direct sunshine, evidently they can endure high
temperatures during aestivation. During a light rain, in E. Crete, the present
author .observed specimens of both A . wiesei and A . inJata, crawling around
(feeding?) on a rock-face together; a few sunny days later specimens of the latter
species were observed, hanging free on the same rocky wall, whereas not a single
A . wiesei could be spotted.
The situation in eastern Crete is exemplary for several areas within the range
of the genus. The 13 Albinaria species occurring here (some of which with
subspecies) are endemic to this part of the island. They are to a certain extent
mutually exclusive, as may be concluded from Fig. lA, B in which 327 1-km
square Albinaria records have been indicated. From this data, the actual ranges
of the various taxa may be derived rather accurately. Thus, for example,
A . wiesei, A . hippolyti arthuriana, A . maltzani, A . praeclara and A . drakakisi (Fig. 1B)
have never been found together. Some of these species have very small ranges.
Where two species are locally sympatric, their habitats may be constricted in the
areas of sympatric occurrence, indicating competitive interactions.
Accompanying shifts in conchological characters, such as size or sculpture, could
not be demonstrated.
The distributional patterns and some ecological characteristics of the Albinaria
species that are found near the village of Kavousi are illustrative. The very
distinctive [conchologically, for example, by its decollate (top whorls
deliberately missing) shell and the V-shaped basal crest] A . rebeli (Fig. 3 ) occurs
on rock-faces in only a single short ravine [Figs 1B (arrow R ) , 21 near the sea,
occupying less than a square km in total range. Albinaria rebeli has not been
recorded in very similar habitats which are found nearby and at many other
E. GITTENBERGER
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Figure 1. U.T.M. maps ofeastern Crete, with 1000-feet contour lines, roughly covering the province
of Lassithi, showing 314 I-km square records of the various endemic Albznariu (sub)sp. Upper map
(A) with closed symbols indicates records of A . inJpafa inzata (Olivier, 1801) [lo-pointed stars],
A. intuta draparnaldi (Beck, 1837) [dots], A . inJufa turgidu Wagner, 1924 [5-pointed stars] and
A . moreletiana (Boettger, 1878) [triangles], and open symbols for A . tcres nordriecki Zilch, 1976
[circles], A . tcrcs extcnra (PfeiKer, 1864) [triangles] and A. teres vermiculatu (Boettger, 1883) [stars].
Lower map (B) shows records of A. drakakisi (Maltzan, 1884) [triangles], A . hippolyti arfhuriana
(Boettger, 1878) [dots], A. maltrani (Boettger, 1883) [stars] and A . praeclaru (Pfeiffer, 1853)
[squares]. Capitals (see the arrows with big capitals) indicate records of species known from less than
10 square kilometres: F, A. fuluula Flach, 1988; L, A. leonisorum (Boettger, 1901); P, A . purpureu
Reitsma, 1988;R, A. rebcli Wagner, 1924; S , A. slurany' Wagner, 1924;W, A . wiesei Gittenberger,
1988.
NON-ADAPTIVE RADIATION
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Figure 2. Upper entrance region of a small ravine near Kavousi. The rocky surface in the
foreground is inhabited by both A . drakakisi and A . tcres nordsiecki, with the former hiding in more
sheltered places than the latter. On the rock-face, on the right, only A . rebeli is found (see text).
places in eastern Crete. At the upper end of the ravine, where the rock-faces
inhabited by A . rebeli change into a soil with (large) rocks (see Fig. 2), two other
Albinaria species are found, namely A . teres (subsp. nordsiecki) (Fig. 4) and
A. drakakisi (Fig. 5 ) . Both can easily be distinguished conchologically by their
teleoconch and cervical sculpture and the internal apertural lamellae. The
former species is found in a variety of habitats, among rocks as well as on more or
less high, open rock-faces in eastern Crete, where it is a very common species
(Fig. 1A, circles). Competitive exclusion is hypothesized as the most likely
explanation for its total absence on the rock-faces in the single small ravine
where A. rebeli occurs, implying a narrowing of its usual habitat there. Albinaria
drakakisi (Fig. lB, triangles) is also a relatively common species, which lives with
A. teres nordsiecki (Fig. 1A, circles) at several sites in eastern Crete; if these species
are found together in aestivation, the latter one dominates the open rock-faces,
whereas the former one is restricted to more humid and sheltered sites. The
present author visited the area near Kavousi on a cloudy day with short periods
of light rain and did not observe a spatial segregation between active A. drakakisi
and A . teres, whereas specimens of both species had not entered the territory of
A. rebeli. It is worth emphasizing here that during the nearly annual periods of
prolonged heavy rains in Crete, A. drakakisi and A . teres will be washed passively
into the small ravine bordered by limestone walls with A. rebeli, apparently
without disturbing the described pattern, although A. teres is found on such walls
at many places nearby.
The principle of competitive interactions resulting not in total exclusion of one
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E. GITTENBERGER
of the associates, but in habitat constriction only, can also be illustrated with
A. praeclara (Fig. 6). This species is very common, being the only Albinaria, both
among rocks on the ground as well as hanging in aestivation or actively crawling
during wet weather, on rock-faces west of Aghios Nikolaos. Without any change
in shell size or sculpture that we could demonstrate, A. praeclaru (Fig. lB,
squares) is found as a strict ground dweller north of this town, where
A. moreletiana (Fig. 7) is the only Albinaria found in aestivation on the rock-faces
(this area has not been studied during wet weather). On the nearby rocky
southern part of the Spinalonga peninsula, where rock-faces are lacking, only
A. moreletiana (Fig. IA, solid triangles) was found, which acts as a ground dweller
here, without showing shifts in conchological characters.
Many Albinaria species occur abundantly and the individual snails are often
not well hidden, but hang free on the rocks. This increases the likelihood of
passive dispersal and, consequently, reduces the probability that allopatry
simply resulted from allopatric speciation not followed by secondary contacts
and competitive interactions. This may also be concluded from the patterns on
Fig. 1, which cannot easily be transposed into (former) geographically isolated
fragments of territory. In fact, the actual ranges of the species and subspecies are
indicative of secondary expansions or reductions. The disjunct range of the rare
NON-ADAPTIVE RADIATION
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Figures 3-7. Front view of shells of Albinariu rebeli (Fig. 3 ) , A . leres nordsiecki (Fig. 4), A . drakakisi
(Fig. 5 ) , A . praecluru (Fig. 6) and A . rnorelefiana (Fig. 7 ) . Figures 3a-7a. The cervical parts of the
same shells. Scale bars for the two series of figures, given on Figs 6 and 6a = 1 mm. Photographs by
A. 't Hooft (R. U. Leiden).
A . leonisorum (Fig. IB, three arrows with L), at both sides of the low area north of
Ierapetra, is difficult to explain without this. Albinaria hippolyti arlhuriana and
A . praeclara may be cited as relatively euryecious Albinarias, that are found from a
few metres above sea level to up to over 1000 m high in the mountains, where
they occur under considerably more extreme conditions, with a snow cover
during part of the winter. It is unclear to what extent the geological history of
the area has contributed to their distributional pattern. However, it seems
probable that their actual, partly disjunct, ranges depend for a considerable part
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E. GITTENBERGER
upon migrations and/or local extinctions, and competitive interactions with
adjoining congeneric taxa occupying similar niches.
The distribution of the various subspecies of A. teres (Fig. lA, open symbols),
which is still unknown in some parts of south-eastern Crete, suggests secondary
shifts in ranges. Afbinaria teres extensa (triangles), for example, is distributed from
north-eastern Crete, along the relatively low area south of Sitia, towards a
narrow zone along the south coast running in an easterly and westerly direction.
The three subspecies of A. teres indicated on Fig. 1A are interconnected by
hybrid zones, except in the extreme south-eastern part of the province of Lassithi
(Fig. 1A, B), where their diagnostic characters are optimally developed and
morphologically intermediate Populations were not found, although the
allopatric ranges come close together here.
The factual observations concerning Afbinariu in nature do not support the
view that these snails have “diversified to occupy a variety of habitats”
(Futuyma, 1979: iv). Afbinaria seems to have diversified into by far the most
speciose genus of the Clausiliidae (Nordsieck, 1979) without much niche
differentiation, to occupy more or less the same or only a narrow range of
habitats. There is no obvious ‘adaptive landscape’ with distinct ‘adaptive peaks’.
The variety of specific combinations of conchological characters, within a
genus that anatomically is not extraordinarily variable, illustrates that there are
many ways to find a solution. A certain niche may be occupied more or less
equally well in various ways. The specific characters, especially the
conchological ones, are most certainly at least partly adaptive, as suggested by
Kemperman & Gittenberger (1988), but the radiation does not deserve that
epithet because the morphological diversity is not paralleled by a broad
ecological differentiation.
It is suggested that the allopatric diversity of both the camaenid species,
reported upon by Solem (1984), and the Albinaria species exemplify nonadaptive radiations. Their distributional patterns are strikingly different from
those of the cichlid fishes in African lakes, which clearly illustrate sympatric
diversity and an adaptive radiation. It cannot be demonstrated that a variety of
potential niches did trigger the Afbinariu radiation.
Probably the stem species of Afbinariu entered a new adaptive zone, where it
managed to live in a n environment which is hostile to most gastropod species, i.e.
dry and warm habitats. At present there is no good, non-dogmatic reason to call
the radiation that followed adaptive. With the available facts it cannot be
demonstrated that each Afbinaria (sub)species “has the morphological or
physiological innovation of the stem species but differs from other species in
character states reflecting adaptations to different niche variables” (Davis,
1981: 1). The least speculative theory is to assume that the radiation in Adbinaria
is (still) mainly non-adaptive. By doing so, the mosaic distributions, mentioned
above, can be looked upon as a result of Gause’s rule and stochastic processes,
maybe with species selection having wiped out certain species nearly completely.
This theory could be falsified by demonstrating that, on the contrary, the species
are adapted to special local conditions, which have a mosaic distribution in the
field, parallel to that of the species themselves. Unfortunately, our knowledge
concerning the phylogeny of the various species is still insufficient and cannot be
used for a better understanding of the observed facts. Physiological and
behavioural studies on Albinaria, including an analysis of the mucus, could also
provide relevant results.
NON-ADAPTIVE RADIATION
27 I
INDIVIDUALITY OF VARIOUS TAXA
The phenomenon of non-adaptive radiation demonstrates once more the
relevance of the individual (genetic) properties of (groups of) species with regard
to their evolutionary potential. Obviously, for a radiation to occur, the
environment does not necessarily have to offer different potential ‘adaptive
peaks’. It can be sufficient that the habitat is fragmented. Non-adaptive
radiation turns out to be a special case of allopatric speciation and a first order
radiation sensu Davis ( 1981) .
What actually happens after the fragmentation of a range and within what
period of time, depends primarily on the specific properties of the taxon
involved, which include its still rather mysterious homoeostatic mechanisms. The
same characteristics apply to cases in which a taxon migrates into an area in
which its preferential habitat is very disjunctly distributed.
Allopatric speciation is not an automatism. Monotypic species may have
disjunct ranges for a considerable period of time. The cave snail Pholeoteras euthrix
(Prosobranchia: Cyclophoridae) , a European Old-Tertiary relict species, is
known from two subranges, separated by a distributional gap (where research
has been done) of c. 350 km (Gittenberger, 1977). It is improbable that this is a
very recent pattern. Gene flow between the populations in the two subranges is
not conceivable. Nevertheless, specimens belonging to the two subgroups cannot
be distinguished from each other taxonomically.
CONCLUSION
Different taxa may differ considerably in evolutionary potential. Stasis,
radiation and transitional states may follow after the origin of a disjunct range
for a certain species. If radiation occurs, this will be more or less clearly adaptive,
non-adaptive or non-adaptive changing into adaptive while the process
proceeds. It is too easy to indicate every radiation as adaptive, simply referring
to those cases in which the impact of adaptation is questionable, as insufficiently
known.
ACKNOWLEDGEMENTS
I am grateful to Dr C. D. N. Barel, Prof. A. J. Cain and an unknown referee,
for their critical comments on this paper.
REFERENCES
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of Mollusca. Malacologia, .?I: 1 4 .
FRYER, G . & ILES, T. D., 1972. The Cichlid Fishes of the Great Lakes of Africa: their Biology and Evolution.
Edinburgh: Oliver & Boyd.
FUTUYMA, D. J., 1979. Evolutionav Biology. Sunderland, Massachusetts: Sinauer Associates, Inc.
GITTENBERGER, E., 1977. Cave snails from Corfu, Greece. In Comunicaciom d e l 8 . Simposium BEspcleologia.
Bioespeleologiat 47-53. Terrassa: Centre Excursionista de Terrassa.
KEMPERMAN, Th. C. M. & GITTENBERGER, E., 1988. On morphology, function and taxonomic
importance of the shell ribs in Clausiliidae (Mollusca: Gastropoda Pulrnonata), with special reference to
those in Albinaria. Basteria, 52: 77-100.
NORDSIECK, H., 1979. Zur Anatomie und Systematik der Clausilien, XXI. Das System der Clausilien, 11:
Die rezenten europaischen Clausilien. Archiu fur Molluskenkunde, 109: 24!+275.
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SMALLRIDGE, M. A. & KIRBY, G. C., 1988. Competitive interactions between the land snails Thebapisana
(Muller) and Cernuella virgata (Da Costa) from South Australia. Journal of Molluscan Studies, 54: 251-258.
SOLEM, A., 1984. A world model of land snail diversity and abundance. In A. Solem & A. C. van Bruggen
(Eds), World- Wide Snails. Biogeographical Studies on Non-Marine Molfusca: 6 2 2 . Leiden: E. J. Brill/Dr
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