Download Competitive speciation

Biological Journal of the Linnean Sqciety, 1 d 225-289. With 3 f Q m
September 1978
Competitive speciation
MICHAEL L. ROSENZWEIG
Department of Ecology and Evolutionary Biology, University of Arizona,
Tucson, Arizona 85721, U.S.A.
Accepted for publication September 1977
A new mode of speciation, competitive speciation, is suggested. It assumes that fitness is
depressed by the density of a phenotype’s competitors, and that the adaptive landscape of
phenotypes is complex. From this it follows that some intermediate forms may be fit if and
only if some extreme forms are rare or absent. Subsequent to the evolution and population
growth of both extreme forms, the intermediate may disappear and homogamy evolve among
each of the extremes because of disruptive selection If so, sympatric speciation has occurred
and niche space has been rendered into discrete segments.
The limitations of the forces leading to competitive speciation are explored. Competitive
speciation is discussed in relation to stasipaaic speciation and host race formation. It may be
responsible for both. Finally the rates of geographical speciation and polyploidy are compared
to those of competitive speciation. The latter should be almost as fast as polyploidy and may be
at the root of adaptive radiation. Unlike either polyploidy or geographical speciation,
competitive speciation accelerates when species diversity declines.
KEY WORDS :-Speciation-sympatric
homogamy-niche.
speciation-stasipatric
speciation-disruptive selection-
CONTENTS
. . . . . . . . . . . . . . .
Introduction
The concept of disruptive selection
. . . . .
Niche discreteness
. . . . . . . . . .
. . . . .
A theory on the origin of gaps niche space
Wrightian surfaces
. . . . . . . . . .
. . . . . . . . . . . .
A scenario
Discussion
. . . . . . . . . . . . . . .
On the roots of disruptive gaps
. . . . . .
Relationships to limiting similarity
Disruptive gaps not necessary or sufficient for speciation
. . . . .
Relationship to stasipatric speciation
. . . .
Gene flow and competitive speciation
Relationship to host race formation
. . . . .
. . .
Tests and rates of competitive speciation
. . . . . . . . . . . . .
Acknowledgements
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Addendum
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References
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275
276
M. L. ROSENZWEIC
INTRODUCTION
Mayr (1963) has elegantly summed up the problem associated with
subscribing to sympatric speciation: in the absence of geographical isolation,
how can homogamy evolve?
Besides the accepted mechanisms involved in polyploidy, the ‘literature
contains two answers to this question: disruptive selection (Mather, 1955 ;
Thoday, 1970, 1972) and discreteness of niche space (Hutchinson, 1968).
However, in the final analysis, both these answers solve one problem only to
create another. The purpose of this paper is to point this out, and to offer a
provisional solution to the two secondary problems (which turn out to be very
closely related). The result is a novel mechanism of speciation incorporating
disruptive selection and explaining a means by which it may appear in natural
circumstances. I propose calling this new process competitive speciation
because, as will be seen, it depends uniquely on competition for the actual
production of new species, whereas all other modes of speciation depend on
competition only for the elimination of excess species after they are produced.
The concept of disruptive selection
Let there be a spectrum of phenotypes of one species. Suddenly some
intermediate phenotypes become unfit. These phenotypes are produced not
only by matings between themselves, but also by matings between phenotypes
of opposite extremes. Because intermediate progeny are unfit, extreme
phenotypes enjoy enhanced fitness if they practice homogamy. Consequently,
reproductive isolation between the extremes evolves and the intermediates
disappear. The result is sympatric speciation.
Natural selection for reproductive isolation is an idea that originated with
Wallace (1889: 173-9). Fisher (1958) added to the concept that genes for such
isolation might exist. Dobzhansky (1940) featured the evolution of reproductive isolation as the final, necessary stage in geographical speciation, but
only later did authors recognize that selection for isolation has the potential to
produce sympatric speciation as well. The theoretical importance of disruptive
selection to sympatric speciation was emphasized by Maynard Smith (1966)
and Pimentel, Smith & Soans (1967). Bazykin (1969) also required it in his
theory. There has been some question as to its ability to foster reproductive
isolation (Scharloo, 1971), but laboratory experiments seem to have confirmed
its potential under stringent rtgimes of artificial selection (Thoday & Gibson,
1962; Coyne & Grant, 1972; Soans, Pimentel & Soans, 1974). Paterniani
( 1 969) disrupted maize into two temporally isolated reproductive races.
Moreover, evolutionary botanists have demonstrated that populations in nature
can actually diverge and become reproductively isolated, and they have
generally attributed this to disruptive selection (Jain & Bradshaw, 1966;
McNeilly & Antonovics, 1968; Antonovics, 1968).
Yet, a realistic field biologist might have been forgiven were he (erroneously)
unimpressed with the importance of Thoday & Gibson’s experiment (as well as
subsequent ones). “How often”, he might have inquired, “will the middle range
of a spectrum of acceptably fit phenotypes suddenly become totally unfit?” In
fact, on the contrary, one might expect the mid-range of such a spectrum to
COMPETITIVE SPECIATION
277
have maximal heterozygosity and therefore be the most fit, and, in particular,
the most adaptable to realistic environmental deterioration. Hence, speciation
by disruptive selection might happen, but one might conclude that unless the
Creator has endowed the earth with a special and mysterious sort of
intermittently available disruptive angel, it probably does not-or at least, does
not much.
Niche discreteness
Hutchinson (1968) hypothesized that some regions of niche space are
subdivided into regions which can and regions which cannot support life.
Phenotypes adjusted for the latter regions would be maladaptive and probably
absent from nature. Other regions of niche space would not be subdivided and
could support all phenotypes. He theorized that the subdivided niches lead to
general agreement among taxonomists about what is or is not a member of a
given species: the members of such a species are easily definable because they
exploit an island in niche space, an island surrounded by maladaptive ways of
looking (hence of living). In contrast to such non-controversial taxa are those
that might be expected to fill an undivided niche space. Because a continuous
array of phenotypes is fit, a continuous array should exist and there will be no
place to draw a taxonomic line. The result is a “difficult” genus, and no end to
discussion regarding its proper systematic treatment.
(Hutchinson carefully entitled his essay “When are species necessary?”
Although good biospecies are not absolutely necessary if niche space is
continuous, they may nevertheless exist as products of geographical speciation
or polyploidy.)
Hutchinson’s thoughts have obvious implications for our consideration of
sympatric speciation. If a way could be imagined for a species occupying a
discrete niche space to colonize a neighbouring niche space, then intermediate
phenotypes between it and its daughter colony would be unfit. This might
produce selective pressure for the evolution of homogamy. In fact, once the
successful colonization had taken place, the species would be in the identical
selective situation as has been produced in laboratories studying disruptive
selection.
Examples of discrete realized niches are known to most field biologists.
Model case histories include leaf-mining insects (Opler, 1974) and tropical
flower mites (Colwell, 1973). Yet, before we can consider discrete niches as
common causes of sympatric speciation, we must answer an important
question. How does the colonization of niche islands take place? Does it
depend upon saltation, or can some more creditable process be imagined which
will “deposit” newcomers on empty niche islands?
A THEORY ON THE ORIGIN OF GAPS IN NICHE SPACE
Wrightian surfaces
I believe that the resolution of both problems-how intermediates become
unfit, and how colonists arrive at tenable niche islands-lies in an examination
of adaptive landscapes of genotypes (Wright, 1932). Simpson (1953)pointed
out that phenotypes and their fitnesses could also be represented by such
278
M. L. ROSENZWEIC
landscapes. Lande (1976) has formalized this, and added the concept of
frequency dependent selection. I shall now propose to consider how landscapes
should change in the face of diffuse intraspecific competition.
Recall that in the Simpson version of the landscape, phenotypes are
represented as points in a Cartesian coordinate system. (Most adaptive
landscapes are drawn with two phenotypic axes, but there could be more or
less.) One axis might represent body length, another, the ratio of jaw length to
breadth, etc. Finally, another axis is added: the fitness of the ith phenotype
(usually this is represented as a third dimension, altitude, but it could be the
second or the fifth or the n + Pt).
In Darwin’s and Wallace’s arguments for natural selection, fitness was the net
rate of reproduction of a phenotype. Population geneticists have come to
realize that other influences such as mutation and genetic structure (e.g.
diploidy) also influence the commonness of phenotypes. In this paper, I shall
assume (with Van Valen, 1974, 1976) that these constraints are relatively
minor. If so, fitness can be approximated by
the rate of change with time
of the natural logarithm of the density of the ith phenotype. This is a poor
assumption for a single locus situation-but see the companion paper by Pimm
(in press) which shows that the conclusions of this paper can hold even for such
a case-however it improves with genetic complexity or restriction to haploid
organisms. With this approximation of fitness, a fitness of zero implies steady
generation by generation replacement and is equivalent t o an arithmetic fitness
of 1.0.
The important property of the adaptive landscape that requires alteration is
its rigidity; except in cases of fluctuation and alteration of the environment,
the adaptive landscape has so far been imagined to be fixed in altitude because
it assumes fitnesses to be constant properties of phenotypes. But fitness is
constant only in that magical universe where resources are infinite. In the real
world, fitness declines as resources become scarce and fitness reaches zero when
density achieves carrying capacity (Fretwell, 1969; Bulmer, 1974). Fretwell &
Lucas (1970) have expanded this concept t o the situation where any number of
phenotypes coexists stably because each exploits its own special subniche. At
an evolutionary and density steady state, each phenotype again has fitness zero
(although different phenotypes may have achieved quite different densities).
Adding the concept of density dependent fitness to the adaptive landscape
converts the rigid topography of Sewall Wright into a dynamic surface, one
whose altitude responds to the pressure of density. The denser a phenotype,
the lower its fitness. In the remainder of this paper, such surfaces will be called
Wrightian surfaces.
One further assumption must be made for this model t o be used in
understanding niche gaps. We must assume that each phenotype exploits not
only its own specialized subniche, but also exploits the subniches of similar
phenotypes, at least to a small extent. MacArthur (1973) terms this diffuse
cornpetition.
A scenario
Now we are ready to envision the origin of niche gaps. Imagine an
unoccupied dynamic Wrightian surface of two axes, one phenotypic, the
second fitness (Fig. 1A). Assume that the lowest fitness on the surface is
COMPETITIVE SPECIATION
279
m
i
1A
I
i
Figures 1 to 3. 1. Development of a disruptive gap. Fitness, I i @ f i is the rate of change of the
logarithm of the density, @j of the ith phenotype. In part A we see the adaptive landscape (top)
in the absence of any density pressure (bottom). In B, phenotypes under the left adaptive peak
have appeared and increased. By C, they have increased in variance and filled the left peak. At
D they have evolved across the adaptive bridge and submerged it, producing a disruptive gap.
2. A blocking gap. This is an alternative to Fig. 1C. It prevents the occupation of the right
adaptive peak.
3. No gap. This is an alternative to Fig. 1D.
greater than zero; in other words, there is no hard selection of phenotypes
(Wallace, 1970) in this system; all phenotypes can survive and reproduce
adequately in the environment. Now we locate adjacent peaks in the surface
and introduce the phenotype corresponding to the f i s t peak. As this
phenotype grows in population, it depresses its own fitness and the fitnesses of
the (as yet non-existent) phenotypes to its right and left. Soon it reaches
carrying capacity (at which density its fitness is zero). At this stage, if its degree
of specialization is sufficient relative to the breadth of its original Wrightian
peak, it has created a dimple in the surface: the fitness of phenotypes to its left
and right are higher than its own. This is tantamount to selective pressure for
those adjacent phenotypes to evolve. Presumably they do since they are only
infinitesimally different from the original. In so doing they exert back pressure
on the special resources of the first phenotype and so reduce its fitness. Its
density must accordingly decrease until its fitness has again climbed back to
zero. At equilibrium, the densities of all three phenotypes are such that all
three have fitness zero. The net effect is to extend the dimple; its indentation is
broader and its shoulders farther apart (Fig. 1B).
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M L ROSENZWEIG
The evolution of phenotypic expansion continues in the same manner until
one of three things happens.
Case I: Blocking gaps. Adjacent, as yet non-existent phenotypes have their
fitness reduced below zero (Fig. 2). In this case the selective pressure for niche
and phenotypic expansion ceases, and the adjacent phenotypes do not appear.
(Or they may appear rarely as mutants. Or they may appear as inevitable
products of the genetic constraints that are required to produce the adaptive
degree of variability, e.g. additive multiple loci.) Essentially, gaps in niche space
appear, but they cannot be crossed without saltation.
Case2: No gaps. The entire phenotypic spectrum evolves and all of its
components are adjusted in density so that their fitness is zero (Fig. 3).
Assuming that the unoccupied Wrightian surface is the least bit bumpy, the
actual genetic system which could produce such a density distribution within
one species at birth must be fairly complex and has not yet been imagined by
science. But a collection of species (produced by geographical speciation or
polyploidy) could do it, and the result might be a “difficult genus”.
Case 3: Disruptive gaps. Between the two peaks of the unoccupied surface is,
by definition, a trough. As the wave of phenotypic expansion approaches this
trough, it may be depressed below zero. This is a Case 1 situation. However, the
depression may not be that severe (Fig. lC), and the wave may succeed in
passing the trough. At that time, competitive pressure on the trough will
emanate both from its right and its left. If the trough is still able to support a
positive density of its phenotype, then we have a Case 2. But if the pressure
from both sides is sufficient to depress the fitness of the trough phenotype
below zero, even when the density of that phenotype is zero, then a gap has
appeared in the niche space (Fig. 1D).
This gap is different from a Case 1 gap in two ways. It does not exist until its
borders are occupied, and, because it is capable of causing disruptive selection,
it can produce sympatric speciation. In what follows, I shall attempt to explore
the biological circumstances which may favour the appearance of disruptive
gaps, and the means by which one might attempt to discover if competitive
speciation has been at all significant. But before doing that, it seems useful to
review the foregoing by introducing an analogy which may be of didactical
value.
The Wrightian surface is like a sphagnum bog. Such a bog is a floating island
of interconnected sphagnum moss, varying in thickness, and therefore, in the
weight it will bear at any given point before that point and a neighbouring
portion of the mat of moss sink below the surface of the water. In this analogy,
weight is like density, position like phenotype, and the water level symbolizes
the zero fitness level. The thickness of the mat is related to the abundance of
resources for the various phenotypes. The interconnectedness of the sphagnum
represents the diffuse competition of similar phenotypes.
The reader should now have a graphic image of what I believe the Wrightian
surface to be like. With zero population density everywhere on it, most or all
the mat is above water. However, some portions of the mat are so thin that
when their thicker surroundings are made to bear supportable densities, they,
the thin portions, sink below the water even without a single individual resting
upon them. Should such gaps isolate an area of thick moss before it is made to
bear density, they are blocking gaps and their isolated island of niche space
COMPETITIVE SPECIATION
281
cannot be colonized by sympatric speciation. But when the isolation of an area
depends upon its supporting phenotypes of its own, the resultant gap is a
disruptive gap, and may induce sympatric speciation.
DISCUSSION
This paper has merely attempted to synthesize well-known concepts, and, by
doing so to emerge with a possible mechanism for sympatric speciation, a
mechanism, moreover, which does not involve any phlogiston or similarly
unbounded leaps of faith. Indeed the Wrightian surface contains a simple
enough explanation of both questions raised at the beginning of the note.
Disruptive discontinuities in niche space may arise as a result of diffuse
competitive pressure emanating from similar phenotypes and exerted on
regions of niche space supported by adequate but not abundant resources. And
evolving across such gaps should present no unusual problem, since the gaps do
not exist until after the evolutionary transition has been successfully
negotiated.
Not all gaps in niche space ought to be disruptive. And not all need be
produced by competitive pressure. For example, it is often pointed out that the
organic evolution of the wheel has never occurred because transitional forms
would suffer hard selection.
On the roots of disruptive gaps
Peaks and troughs in an unoccupied Wrightian surface might be caused by
the abiotic discontinuities with which the earth seems well supplied. The
protoamphibian, Eusthenopteron, clambering around between ponds during
the Devonian might have been capable of dealing with the terrestrial
environment which it traversed. Yet it is not difficult to imagine the
improvements which would (and presumably did) lead to its replacement by a
descendant more impressively adapted to deal with the new and harsh demands
made on a vertebrate by a terrestrial existence.
Somewhat less dramatic resource discontinuities might also produce effective
Wrightian surface relief. Prof. R. Alexander (pers. comm.) has imagined a
short-grass prairie katydid population expanding towards the sagebrush filled
Great Basin Desert. The prairie forms were probably able to manage in the
desert, but the selective pressure on them to change from their grassland form
to a properly adapted desert phenotype was apparently intense. Intermediates
have vanished.
Throughout this note we have referred to fitness in the unoccupied
Wrightian surface as if it were proportional to the abundance of specialized
resources in each subniche. Indeed this is one reasonable interpretation, and
multimodal variations in the abundance of the specialized resources of each
subniche would seem to be one means of generating surface relief. However, it
is important to emphasize that the previously suggested examples did not
depend on that. In fact, in those cases, intermediate forms exploited the same
resources as their more extreme successors. What produced their replacement
was not any lack of abundance of their own subniche’s opportunities, but their
own compromising intermediacy.
282
M
L ROSENWEIG
Relationship to limiting similarity
There is one important concept which although a potent producer of
phenotypic gaps, does not lead to disruptive gaps, and that is the principle of
limiting similarity (MacArthur & Levhs, 1967). May & MacArthur (1972)have
shown that two species cannot coexist if their niches overlap beyond a certain
amount, called the limiting similarity. Thus it might be erroneously concluded
that, given even a unimodal or an equitable distribution of resources, an array
of exploiting phenotypes will contain whatever discontinuities are necessary to
prevent their infringing the limiting similarity. However, limiting similarity is a
concept that applies only t o different species. It depends upon the stochastic
variation in resources and environment that extinguishes whole species. A
deterministic model contains no limiting similarity; overlaps which are even
minutely different from 100% prevent extinction (May & MacArthur, 1972).
Hence, if we are dealing with phenotypes of one species, subniches may be
infinitely close, because a phenotype which disappears by accident is replaced
almost instantaneously by the interbreeding of remaining phenotypes.
Disruptive gaps not necessary or sufficient for speciation
Despite the postulated importance of islands in Wrightian surfaces, such
islands are neither necessary for speciation in general, nor sufficient for
competitive speciation in particular. Let us first examine the former.
Anyone convinced that either polyploidy or geographical speciation occurs,
recognizes that gaps are not necessary for speciation. Products of polyploidy
are automatically poor at crossing with their parent species; products of
geographical isolation may not be compatible because although they have
solved the same problems of adaptation, they have done it with different gene
complexes and fine structures. Moreover two species not separated by a niche
gap may continue to coexist, so the absence of a niche gap does not even imply
the failure of the products of speciation. For example, the genus Empidonax
(Aves: Tyrannidae) contains a collection of several cryptic species which even
the most able birdwatchers dare not try to distinguish except by song (i.e. a
device for homogamy). In another case, Colwell (1973)described the ecology
of two species of tropical mite which reproduce in flowers peculiar to each. Yet
he showed that each could feed and reproduce successfully on the other’s
flower. So the ecological significance of their difference is negligible. Instead
the mites are probably using the flower differences as a device to maintain their
homogamy .
There are at least two reasons why disruptive gaps may prove insufficient for
speciation. One is that a species faced with such a gap may respond with a
classical discrete polymorphism rather than with homogamy (Mather, 1955).A
related alternate response is polytypism. Significantly, Heed (1963)found that
the variety of Drosophila morphs in different places is similar, but that in some
places the morphs were of the same species, whereas in others they were of
different species. The circumstances which would favour the one or the other
response seem worthy of investigation. From his studies on sockeye salmon,
Oncorhynchus nerka, J. R. Calaprice (pers. comm.) suggests that polymorphism
should be the more suitable response if the environment is so unstable that one
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283
of the subniches sometimes vanishes for a while, or if catastrophes can befall
the occupants of any subniche without affecting the occupants of the other(s).
A second reason is that a species faced with an opportunity may not be able
to expand its phenotypic variance sufficiently quickly to take advantage of
unfilled subniches (Slatkin, 1970). This may be a serious genetic constraint to
competitive speciation, although Slatkin’s results depend on the assumption of
random mating.
Relationship to stasipatric speciation
In the past decade, investigators have been examining a new mode of
speciation called stasipatric by M. J. D. White (1968). It appears to have
occurred at least in sedentary grasshoppers (White, Blackith, Blackith &
Cheney, 1967), walking sticks (Craddock, 1975) and placental mammals
(Wilson, Bush, Case & King, 1976). In stasipatric speciation, a chromosomal
mutation originates somewhere deep in the range of a species. The new
homozygote is the fittest in some portion of the range and- takes over. The
result is two races, each occupying a fraction of the former total range. There is
some disagreement whether these are properly termed different species,
because when their ranges abut, the two sometimes hybridize naturally (Key,
1968). But natural hybrids do suffer in fitness owing to aneuploidy.
The principal theoretical problem with stasipatric speciation is that no one
has proposed a mechanism to allow it to pass through its earliest stage when all
of the new mutant chromosomes are in heterozygous form. Key (1968)
recognized this problem quickly and surmised that the new chromosomal races
must originate allopatrically “by random fixation in very small, completely
isolated colonies”. Wilson, Bush, Case & King (1976) propose that the random
fixation may take place in small, socially isolated groups. In general, efforts to
account for stasipatric speciation without genetic drift have failed. White (in
press) tested the idea of meiotic drive, but it also failed.
However, I believe that White was on the right track. One must attempt to
account for stasipatric speciation by considering what advantages accrue to the
new mutation that counterbalance its disadvantage in meiosis. I suggest the
answer may lie in the Wrightian surface. When the new mutant is rare, it does
not face competition from the new homozygote (because the latter is virtually
non-existent). However, since this new homozygote is to be favoured, it may
well be that the new heterozygote has sufficient of the homozygote’s
properties t o outperform the old homozygote in part of the range. If so, the
new chromosomal arrangement will increase in frequency and produce
homozygotes. Only then will the heterozygote be outdone.
If all this sounds like competitive speciation, it should. I propose that
stasipatric speciation is a particular type of competitive speciation defined by
its chromosomal events. Undoubtedly stasipatric speciation often results in the
evolution of homogamy. When it does not, the individuals appear quite
sedentary (Bush, 1975) which suggests that for these forms, location itself is
almost always a sufficient reproductive cue to produce homogamy (thus
obviating the need for further refinement in the mechanism of mate selection).
For this to be true, natural selection against a homozygote in the wrong place
must be severe, severe enough in fact to preclude the fuzzing of the sharp lines
that separate the parapatric races.
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M. L ROSENZWEIG
Gene flow and competitive speciation
Although extreme sedentariness may, as I have argued, abort the completion
of competitive speciation, I certainly do not mean to imply that any degree of
gene flow, however high, is supportive of it. Totally unrestricted gene flow
should instead force phenotypes to adapt t o some average expectation; to some
intermediate niche which might be termed the dominant opportunity (Levins,
1962). Although the principal point of this paper is to argue only that
competitive speciation is possible at intermediate levels of gene flow, it seems
worthwhile t o suggest some of the ways in which such levels might be realized
in nature.
The obvious ways are low vagility or its formal equivalent, a semipermeable geographical barrier (Slatkin, 1973). It should not bother one in the
least that the latter may suggest a continuum exists between pure sympatric
and pure allopatric speciation. In fact, the compulsive pigeonholers among us
may find nothing but pure frustration in their attempts to draw sharp dividing
lines between sympatric and allopatric processes. The important thing is to
understand the biology even if it is complex and more or less fuzzy.
Complete geographical barriers also cut off gene flow. Mayr (1954,1967)
has emphasized the great importance of this in allowing populations to adapt to
diverse local conditions, and even to radically new niches. Certainly this process
is always allopatric. However, sometimes, speciation following the erection of
an isolating barrier proceeds with extraordinary rapidity. Assuming they are
new species and not relics, the 4 species of cichlid fishes in Lake Nabugabo
constitute such a case; Lake Nabugabo is an isolate of Lake Victoria no more
than 5000 years old (Greenwood, 1965). Perhaps such speed is to be
understood as a result of the colonization of a heretofore unattainable adaptive
zone in a Wrightian surface. If so, the successful colonist may, when it
reinvades the main geographical area, require disruptive selection to complete
its reproductive isolation. Thus whereas there may be times when, in the
absence of geographical isolation, competitive speciation will be thwarted by
too much gene flow, those will also be the instances which spawn cases of
allopatric speciation which would be incomprehensibly rapid were we not to
invoke the directional selection and disruptive selection at the heart of
straightforward competitive speciation. Again, the philosopher’s desire for
simplicity may be forced to yield to the biologist’s insistence that nature be
understood on her own terms be they clear cut or not.
Although neither resource nor habitat selection actually reduces gene flow,
each reduces its maladaptive consequences. I doubt this has been fully
appreciated. Gene flow can halt adaptation to specific subniches or t o
restricted, but special environments (Levins, 1965), only because, and onZy if
individuals are fine grained. If they are, they must adapt to some average
environment, to the dominant opportunity (Levins, 1962). If they are not,
then adaptations to more restricted opportunities may also be optimal
strategies if the individual with each special phenotype can seek out the set of
resources or habitats that optimizes its fitness.
Different organisms do not have equal abilities to be coarse grained. Pursuing
consumers (as contrasted with searchers) must be more selective (MacArthur
and Pianka, 1966). Therefore they should also be capable of more certain and
COMPETITIVE SPECIATION
285
more rapid competitive speciation than searchers. Lacking much ability to
habitat select should also impede one’s chances to undergo competitive
speciation. For example sessile organisms like most plants are probably poorer
candidates for competitive speciation than mobile ones like small mammals.
Perhaps the known propensity of small eutherian mammals to habitat select
(Rosenzweig, 1973, 1977; Brown, 1975; M’Closkey & Lajoie, 1975;M’Closkey
& Fieldwick, 1975; Schroder & Rosenzweig, 1975; Deuser & Shugart, 1977;
Whitford, Dick-Peddie, Walters & Ludwig, in press), is at the root of their
ability t o undergo rapid, frequent chromosomal evolution. Wilson et al. (1975)
pointed out the latter fact, but attributed it to social organization. (Of course,
that too can reduce gene flow if the societies are largely endogamous.)
Just as different types of organisms should support competitive speciation
according to their abilities to associate different phenotypes with appropriate
subniches, so different environments should succour competitive speciation to
different degrees. The more productive an environment, the more it encourages
habitat selection (MacArthur & Pianka, 1966; Rosenzweig, 1974). Thus there
ought to be a latitudinal gradient of competitive speciation rates, with tropical
environments fastest. This affords yet another potential cause of the well
known latitudinal diversity gradient (see Rosenzweig, 1975, for a reorganization of others according to extinction and origination rates).
Relationship to host race formation
Bush (1969) provides instances of sympatric race formation which may also
turn out to be explained by Wrightian surfaces. Here races of tephritid flies are
formed which emerge at different times according to the reproductive season of
their host plant. To account for this, Bush proposes saltation, although he
softens the blow by presupposing that major changes in emergence time can be
accomplished with only minor alterations in genes. Indeed Huettel & Bush
(1972) claim t o have demonstrated that the difference between two species of
Procecidochares is due to one major allele. However, their results are just as
easily interpreted as due t o one major chromosomal mutation, and a
chromosomal rearrangement is a good way to allow the gradual reorganization
and replacement of a complex of genes. It would seem at least as plausible to
dispense entirely with the need for saltation, and notice instead that in the
absence say of a race of Rhagoletis indifferens adapted to domestic cherry,
those emerging last out of a wild cherry race would be favoured because they
could tap a new resource, a few early domestic cherries. As their kind increased
and evolved toward even later emergence, the original late-emerging wild cherry
forms and bridge-time forms would be outcompeted. A regime of disruptive
selection could then isolate the host races completely.
Host races and species are quite common in insects (e.g. Eastop, 1972;
Knerer & Atwood, 1973). In many such cases, the hypothesis that their
formation was due to competitive speciation, appears to fit the data as well as
it does for tephritid flies.
Tests and rates of competitive speciation
That gaps are neither sufficient nor necessary for speciation is not
bothersome providing it can be shown empirically that competitive speciation
286
M. L. ROSENZWEIG
is the likely mechanism behind the production of some species. One might also
like to know if it has been a significant contributing factor in the diversification
of the world’s biota (or any part of it) as compared to polyploidy and
geographical speciation.
Previously I have tried to explain stasipatric speciation and the formation of
sympatric host races by Wrightian surfaces and competitive speciation. Implicit
in this explanation has been that some competitive speciations are recent
enough to be reconstructed. If so, hybrids should be able to outcompete
homozygotes forced to exploit the resources or habitats of the other
homozygote. Dr W. Heed and I hope to undertake such a test in Drosophilu.
Hopefully others will be started in other taxa.
Another feature which distinguishes competitive speciation is its rate. While
not instantaneous, it must be much faster than geographical speciation. Host
races have certainly formed in historic times (Bush, 1969). And, once
directional selection has produced the new variety, disruptive selection requires
only about ten generations (more or less) to do its work (Thoday & Gibson,
1962; Paterniani, 1969). Hence the principal rate limiting step is probably the
directional selection of the new form. Notice, however, that the disruptive
selection need not wait for the perfection of the new form. As soon as enough
progress has been accomplished to outcompete intermediates, the new form
should become reproductively isolated.
The rate of competitive speciation responds uniquely to changes in species
diversity. Elsewhere (Rosenzweig, 1975), I argue that neither geographical
speciation nor polyploidy accelerate when empty niches become available. On
the contrary, their total rate almost certainly declines after species become
extinct. But competitive speciation is different. Should a species occupying an
island on a Wrightian surface become extinct, its niche is reunited to another
and a new speciation event is encouraged. It is therefore easier to understand
the phenomenon of adaptive radiation in terms of competitive speciation than
in terms of other speciation mechanisms. Low diversities produce high rates of
competitive speciation even though rates of polyploidy and geographical
speciation decline.
ACKNOWLEDGEMENTS
My thanks to R. Alexander, J. R. Calaprice, W. Heed, G. Mark, H. R.
Pulliam, W. M. Schaffer, G . G. Simpson, J. M. Smith, M. SouK, L. Van Valen
and M. J. D. White for conversations and suggestions. NSF grants supported the
research. An abbreviated version of this paper was first presented to the Society
for the Study of Evolution at their New Orleans meeting, May 1976.
ADDENDUM
After the first public presentation of this paper, it became apparent that
many others had been developing similar ideas. G. G. Simpson (1953) wrote of
the colonization of new adaptive zones and the subsequent disappearance of
intermediates because they were “relatively ill-adapted” (pp. 158, 392). His
primary purpose was to adduce empirical cases which had demanded rapid
evolution to a new adaptive peak (“quantum evolution”), but it seems clear
COMPETITIVE SPECIATION
287
that a mechanism similar to the one I have herein outlined was also on his
mind. In the spring of 1977, I was privileged to see Pimm’s work on the subject
which certainly contains the same mechanism. Finally, both Tauber 8t Tauber
(1977) and Endler (1977) have published somewhat more restricted but quite
comparable mechanisms.
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