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Reprinted With permission on one of the Contributions from the Scripps
Institution of Oceanography, University of California, New Series.
Reprint from
VERTEBRATE SPECIATION
A University of Texas Symposium
Isolating Mechanisms in the
Speciation of Fishes.
•CARL L. HUBBS
Scripps Institution of Oceanography,
University of California
THAT THE PROBLEM of segregation versus integration is one of long standing will be obvious from the fact that
I treat it as it is exemplified among the lowest of the vertebrates.
Speciation in its early stages obviously results from the ascendancy
of segregation, as integration is reduced and eventually eliminated.
(I hasten to add that I derive no moral from this concept, and draw
no comparison with any current social problem.)
We may visualize speciation as a long-continued and often fluctuating conflict between forces that tend to unify the gene pool and
those that tend to diversify populations genetically. The prime unifying force is interbreeding. The opposing factors, which lead to genetic
isolation and speciation, are, I believe, numerous and complex; they
are both intrinsic, in genetic mechanisms, and extrinsic, in ecological
relations.
I belong to the school that stresses what may be called the environ-
1 Contributions from the Scripps Institution of Oceanography, University of
California, New Series.
Comparative Isolating Mechanisms
mental potential as a central factor in speciation, hence as a major
force determining the rate of genetic isolation. I shall, therefore, place
more emphasis on the ecological factors than on the genetic mechanisms as such.
Blocks to Interspecific Hybridization in
Nature
Discrepancy between genetic potential and
the facts of life is dramatically exemplified by the extreme infrequency of hybridization in nature between species that can readily
be cross-fertilized or that interbreed freely on isolated pairing in
aquaria.
In the perch family, Percidae, for example, interspecific hybridization in nature is rare, in fact, extremely rare except among some of
the more primitive darters, such as Hadrcrpterus maculatus and Percina caprodes. Yet Clark Hubbs has produced numerous hybrid combinations, almost at will, by appropriate juggling of gametes. Many
of the darters live together on the same riffles, and breed in similar
fashion and at the same time. We can only assume that minor but
effective behavioral differences—habitudinal and psychic—segregate
the breeding fish. That a parallel situation holds for the oviparous
cyprinodonts has just been indicated by Clark Hubbs. He is also
vigorously attacking the problem of reduced interspecific fecundity
in regions of sympatry.
The same phenomenon is exemplified by viviparous fishes, with
complicated intromissive organs, that pair in highly evolved patterns.
Thus the two best-known species of Xiphophorus, hellerii and maculatus ( until recently referred to distinct genera), have been crossed
by forced isolated cohabitation thousands of times in the aquaria of
fish geneticists and fish hobbyists, and the other species referred to
the same tribe and now to the same genus often interbreed freely
and produce fertile offspring under such conditions. Although many
thousand specimens of Xiphophorus have been collected and critically examined from many localities, so far as I know not a single
natural hybrid has appeared. Gordon ( 1957 ) came to the same conclusions. To be sure, some of the species of Xiphophorus are geographically isolated, but the ranges of maculatus and hellerii overlap
very widely, and these species often occur in the same pond or same
stream section ( though they are more often isolated ecologically).
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Isolating Mechanisms in the Speciation of Fishes
In the extensively studied genus Mollienisia—or if you wish, spell
it Mollienesia, or lump the genus with Poecilia—we have found natural interspecific hybrids, but in extraordinary rarity. Thus between
species of the Mollienisia sphenops and the M. latipinna species
groups, fewer than ten hybrids have been encountered in nature,
though the species pair and hybridize freely ha isolated aquarium
matings. These natural hybrids have involved M. mexicana of the
short-finned sphenops group and the long-finned species velifera and
petenensis. Hybridization in the past between these two species
groups was presumably involved in the origin of the renowned allfemale, matroclinous Amazon molly, Mollienisia formosa ( Hubbs and
Hubbs, 1932). ( Clark Hubbs and associates [1959] have recently
taken in nature a few genetically female, phenotypic males of this
peculiar, genetically isolated type.)
The factors that so effectively block miscegenation between related
poeciliid species must be subtle. The highly complicated copulatory
apparatus is sufficiently similar among the species of Xiphophorus
( Gordon and Rosen, 1951) to provide, in my opinion, no plausible
block to cross-fertilization, and the gonopodial structure is virtually
identical among the species of Mollienisia. Within each group the
mating behavior is very similar, though not wholly identical, as Clark,
Aronson, and Gordon ( 1954 ) showed in commendable detail for
Xiphophorus and as we have observed in Mollienisia. Whether the
matings be between isolated pairs or between pairs in mass matings
involving both sexes of both species, sexual inhibitions seem to be
of limited effect.
In one experiment, in which we kept together ten males and ten
females of Mollienisia latipinna and ten males and ten females of a
species of the sphenops group, counts of the ever-occurring copulatory thrusts showed no preference of intraspecific over interspecific.
Yet all the young produced were from matings within the sphenops
type. Some physiological advantage may accrue in the mating of
intraspecific gametes or in the development of the nonhybrid embryo—but the advantage is certainly not complete in the sense that
normal germ-cell mating and development precludes the hybrid, for
we have had single broods of mixed male parentage, one of which
was produced by a female collected in nature in a pregnant condition. (The one negative experiment in mass miscegenation just mentioned was somewhat abortive and needs to be repeated.)
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Comparative Isolating Mechanisms
Even more striking than this contrast between natural and aquarium hybridization between species of the long-finned and short-finned
groups in Mollienisia is that between two species that have been
confused under the name Mollienisia sphenops. I now have found
that over the middle of the vast range of the sphenops group, from
the region of Veracruz to Costa Rica, two species occur, each in an
almost endless array of local differentiates. One species, which I have
just checked as the true sphenops, has the inner teeth tricuspid; the
other, which may take the name M. mexicana, has these teeth unicuspid. This sounds like a generic difference, but the two types,
though they seem very seldom to hybridize where they occur together in nature ( as they frequently do), cross without restraint in
aquaria to produce apparently perfectly fertile offspring.
The hybrids between species of the sphenops and latipinna series,
in contrast, are characterized by reduced fertility in the female.
Hybrids between species of Mollienisia and those of related genera
in the tribe Poeciliini, occasionally obtainable by aquarium matings,
produce offspring in which the females are infertile and the males
are apparently always incompetent. We might assume that somehow
selection has operated to prevent such miscegenation, but this concept is difficult to apply to crossings within the sphenops complex.
Behavioral Blocks to Hybridization
Some factors, presumably behavioral, block
interspecific hybridization in nature between species that are quite
capable of miscegenation. I suspect that these factors are in part
genetic, the result of selection against the varied inefficiencies of
cross-mating, and in part nongenetic, perhaps also as a result of
selection, in that advantageous patterns of behavior without a special
genetic basis may become established continuously.
We have found that the blocks to hybridization are often broken
down when fresh-water fish species previously separated geographically ( or microgeographically ) are brought into cohabitation. Thus,
we have found hybridization to be unusually frequent where one
species of sucker was led for the first time into habitation with another species through a spillway in the Owens Valley aqueduct in
California, and where species of the Mississippi drainage have become established, presumably through escape of bait, in the Colorado
River system ( Hubbs, Hubbs, and Johnson, 1943). Here another
8
Isolating Mechanisms in the Speciation of Fishes
factor, that of the great scarcity of one species in an abundance of
another, decreasing the chance for homogeny, may be a contributing
or even the controlling basis for the miscegenation. To the degree that
this factor of relative numbers operates, we may regard reasonable
numbers of both cohabiting species as a factor blocking undue interspecific hybridization.
The reality of this factor of unbalanced abundance seems to be
further indicated by the very high incidence of hybridization characteristic of some species, like Clinostomus elongatus, that seem to
be approaching extirpation in the disjunct populations now remaining.
Somehow it seems almost as if species through experience learn
how to behave so as to avoid miscegenation, for the members of a
given species pair may seldom hybridize where they have lived in
contact for a long time, but break down the barrier to miscegenation
where they have just been thrown together. Thus, we have encountered unusually high incidences of hybridization where one sunfish
species was stocked in a lake previously populated only by other
species, but here again the factor of unbalanced population numbers
may have played a role ( Hubbs and Hubbs, 1933). Clark Hubbs is
attacking experimentally the problem of behavioral blocks to hybridization.
Very striking is the picture of natural hybridization between carp
and goldfish. These representatives of quite distinct, though related,
genera live together over much of eastern Asia, including Japan, in
a wide spectrum of relative abundance and in a wide range of habitats, with virtually no natural crossing. Cross-fertilization, however,
is readily accomplished in artificial settings, and in the Lake Erie
drainage these species interbreed in great profusion. After its introduction about seventy-five years ago, the carp found the waters
about Lake Erie so agreeable that a large population developed and
has continuously maintained itself. Later goldfish were flushed into
a Lake Erie tributary by floodwaters and they likewise built up a
large population. Here the two species hybridize very freely. In
places the hybrids, though at least normally infertile, actually outnumber the parental species. ( The same situation has been found
among the sunfishes, and seems to be explainable on the hypothesis
that the heterotic hybrids stem currents more freely than do either
parental species, and thus tend to segregate themselves.) At the start
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Comparative Isolating Mechanisms
the few goldfish may have encountered an overwhelming abundance
of carp, thus greatly increasing the chance of heterogeny; but for
many years both species have been abundant, existing in relative
numbers that surely could be duplicated in many places in Asia,
where the species have somehow learned not to cross, or have developed genetical bases for homogeny. But if the bases for homogeny
had become ingrained into the species, they must have become lost
or rendered ineffectual during at most a few centuries of man-induced
isolation.
The possibility that carp and goldfish once hybridized in China
( and perhaps occasionally still do) and the possibility that the hybrids are occasionally fertile are indicated by the occurrence there of
the genus Carassiops, with intermediate characters largely matching
those of the carp x goldfish hybrid. Other characters, however, indicate that Carassiops, though possibly of ancient hybrid origin, is not
in itself a hybrid.
Hybridization between fish species in nature is frequent, so far as
is known, only among fresh-water species in northern regions, where
ecological conditions and species associations have fluctuated greatly
in response to Glacial and Pluvial events ( Hubbs, 1955). This situation is comparable to that in plants, between which hybridization
has been shown by Edgar Anderson ( 1949 ) and others to be particularly frequent where the ecological conditions have been markedly altered by natural or artificial activities. In tropical regions and
especially in the tropical seas, interspecific hybridization seems almost
unknown, despite ( or perhaps because of) the great multiplication
of species and the great diversity of habitat. In this connection I
would like to express the opinion that Gordon ( 1957 ) and others have
been unduly cautious about accepting any interpretation of fish
hybrids not yet verified by experiments or by study of gonads. Clark
Hubbs is finding some indications that the duration of sperm activity
may be one of the factors affecting the frequency of hybridization.
Blocks to Hybridization and to Viability
and Fertility of Hybrids
Genetic isolations are effected to varying degrees by the development of various blocks to the act of cross-mating
and to the viability and fertility of such hybrids as may be produced.
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Isolating Mechanisms in the Speciation of Fishes
Such blocks have been noted in certain fish hybrids. Heterogenetic
crosses, as between families, may produce embryos, either with or
without indications of paternal gene contribution, but normal young
do not eventuate.
Among the rather freely hybridizing centrarchid fishes, particularly
among sunfishes (Lepomis in the broad sense), the hybrids are almost invariably sterile and are predominantly males with abnormal
spermatogenesis ( Hubbs and Hubbs, 1933). Occasional sunfish hybrids, however, appear to be somewhat fertile. In other groups the
incidence of hybridization varies, and the hybrids show varying degrees of viability and fertility. No sharp line can be drawn between
more or less free gene flow within species and complete blocks between species. Under appropriate stimulus and favorable conditions
species and even genera of fishes produce fertile offspring.
I have already spoken of the seemingly acquired blocks to hybridization in nature between species and between genera, such as Carassius and Cyprinus, in regions where they have long been sympatric.
Carassius x Cyprinus hybrids seem to be normally infertile, because
their characters are consistently intermediate, but there are some
suggestions of occasional fertility.
Other well-defined species seem to produce quite fertile offspring,
for all gradations between them are found in nature. Such gradation
characterizes the frequently produced hybrids between Chrosomus
eos and Chrosomus neogaeus ( the latter until recently regarded as
generically distinct), as also the hybrids between Notropis cornuta
and N. rubella, which very often interbreed as a result of a chance
meeting of sperm and egg when rubella is spawning in midwater
over a breeding group of cornuta ( Raney, 1940). The creek and lake
forms of Siphateles obesus, though formerly regarded as generically
distinct, often hybridize and in some lakes have fused ( Hubbs and
Miller, 1946). Where the appropriate habitats of the two parental
types are available hybridization is limited, but under intermediate
conditions they intermate freely.
Differential habits and habitats are commonly the isolating factors.
By such means, no doubt, the Californian minnows Hesperoleucus
and Lavinia ordinarily maintain their full distinctness in breeding
and in morphology, seldom hybridizing. In one desiccating section of
the San Juan River of the Salinas system, however, where they had
been thrown into cohabitation in dwindling pools, they fused to form
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Comparative Isolating Mechanisms
a hybrid swarm, much like those observed sporadically between plant
species. In working over a very large series Dr. Robert Rush Miller
and I thought we could recognize about five per cent as Hesperoleucus and about an equal minimal number as Lavinia, but on more
thorough study even these few fish showed some evidence of introgression.
In general, the various effective blocks to hybridization are developed roughly in proportion to the degree of systematic divergence
( Hubbs, 1955). This relationship was nicely illustrated in our longcontinued but still largely unreported experimental studies of hybridization in the poeciliid fishes of the tribe Poeciliini. The various forms
of Mollienisia mexicana and of M. sphenops cross freely and produce
fully fertile offspring, in matings both within and between these
closely allied species. Species of the M. sphenops group (including
mexicana) rather readily cross in aquaria with members of the M. latipinna group (latipinna, petenensis, velifera), but the hybrids are
not completely fertile: the male hybrids are almost fully fertile, but
the females are ordinarily sterile. Species of Mollienisia and Limia
occasionally produce hybrids, of which the males are sometimes
fertile, the females apparently never. Mollienisia very rarely crosses
with the less closely related genus Lebistes, and both sexes of the hybrids seem infertile. No hybridization whatever could be effected
between any member of the tribe Poeciliini and any species of any
other tribe. Aquarists often report such heterogenetic crossings, but
on frequent checking I have never verified such a report. In general,
I have found that natural hybrids are produced only among closely
related genera, such as may be classed in one tribe ( Hubbs, 1955).
Within limits there seem to be some exceptions to the rule that the
incidence of hybridization is positively correlated with degree of
relationship. Some very closely related species that are largely sympatric appear to have developed effective blocks to hybridization,
whereas one or both may hybridize rather freely with a less closely
related form with which it is much more restrictively sympatric.
Thus, Notropis spiloptera seems virtually never to cross with its very
near relative N. whip phi, with which it widely occurs, but does cross,
at times, with the less similar species N. lutrensis, the range of which
it overlaps much less widely.
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Isolating Mechanisms in the Speciation of Fishes
Resistance to Genetic Swamping
A considerable body of evidence indicates
that various factors minimize the swamping effects of hybridization
and thus retard or even circumvent this major block to genetic isolation and speciation. These factors seem to exert a force that maintains
taxa, as though pulling them apart, despite the force of interbreeding
that tends to break down the differentiation of these taxa, by causing
them to fuse. No doubt these opposing forces interact variously, so
that the trend toward integration at times and at places is dominant,
whereas on other occasions and elsewhere the trend toward segregation takes over. Let us consider some cases that seem to illustrate this
grand interplay.
In the Lahontan Basin two minnows now referred to the genus
Siphateles behave quite variously in respect to their mutual genetic
relationships ( Hubbs and Miller, 1948). One form, obesus, is characteristic of streams, where it feeds on insect larvae and other bottom
invertebrates and gets along with fewer than twenty stubby gill-rakers. The other form, pectinifer, is adapted to lacustrine conditions
and presumably evolved in the vast Pluvial Lake Lahontan. Its large
size, strong build, upturned mouth, and its very numerous and long
rakers fit it for life in open waters and for feeding on plankton ( which
is much richer in lakes than in streams). The differences are so great
that a conservative ichthyologist ( Snyder, 1917) erected a distinct
genus ( Leucidius) for the lacustrine form. However, in line with
our finding that adaptations to differential feeding are apt to be
terminal phenomena of no great phylogenetic significance, we now
know that these two very diverse forms frequently interbreed—hybridize or intergrade depending on one's point of view. ( We now
put them not only in the same genus but also in the same species,
Siphateles obesus.) In some now confined waters, like Eagle Lake,
the two forms have completely fused to produce a strictly intermediate type. In the larger and more diverse Lake Tahoe intermediate stocks as well as populations of each type exist. Various degrees
of intermediacy are exhibited by local populations. In Walker Lake
near the mouth of Walker River a population essentially uniform in
the characters of the lake form includes a small proportion aberrant
only in the gill-raker character, in which respect some are like obesus
and others are variously intermediate ( indicating past introgression,
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Comparative Isolating Mechanisms
exhibited only in the gill-raker character probably because relatively
few genetic factors are involved). Yet over the basin as a whole the
two forms maintain their distinctness in character and habitat, though
there are in general no impassable barriers to gene flow. Moreover,
the hybridization seems to have been proceeding for many centuries,
because some of the mummies from ancient, dated Indian caches
appear to be hybrids. Some factors, here as elsewhere, must counter
gene interflow in this complex, in which the intergrades ( or hybrids)
must be fertile.
Another case of resistance to gene interflow, worked out first by
Boyd W. Walker and me and more recently by Caryl P. Haskins, is
that of the two northern subspecies of Gambusia affinis, which in
many respects other than geographical intergradation are more distinct that many good species in the Poeciliidae. G. a. holbrookii inhabits the Atlantic Coast and peninsular Florida. G. a. affinis ranges
through the Mississippi Valley to the Rio Grande. Between the Mississippi Delta and peninsular Florida the two forms have been
brought into cohabitation by connecting waters near the coast, and
here they intergrade. The intergrades, like most interspecific hybrids
( and one could call them such if he wished), are intermediate in
nearly all characters, including several trenchant peculiarities in gonopodial characters and in the sensory canals and pores of the head.
But in the fin-ray formulas they combine the numbers of the two species in about equal frequency, apparently because in this species the
fin-ray number, unlike almost all systematic characters, seems to depend on a single genetic factor: the dorsal fin has either six rays as in
affinis or seven as in holbrookii, and the anal fin has either nine rays as
in affinis or ten as in holbrookii. The reality of the interbreeding and
the type of inheritance has been verified by experiment. The intergradation has doubtless existed in this limited area for many centuries, without evidence of extensive gene flow either into the Florida
Peninsula or into the delta region of the Mississippi Valley. And, more
dramatically, the headwater populations of certain streams, some
only a few miles long, have remained essentially pure—of affinis to
the westward and of holbrookii to the eastward.
Something has blocked the gene flow, even within very short distances, between the pure subspecies stocks and the intergrades. It is
almost certain that no gross sterility factors are involved. The fact
that the pure populations of each subspecies occupy headwaters
14
Isolating Mechanisms in the Speciation of Fishes
argues against any special adaptation of either to headwaters. Seemingly there must be some inherent advantage that allows the pure
subspecies to outbreed the intermediates and to build up populations
large enough to block the spread of the intermediates. The extreme
restriction of the population of hybrids between Gambusia affinis and
G. heterochir, so nicely demonstrated by another and now more productive Hubbs ( 1957 ), bears out this interpretation.
The force that resists swamping ( and even probably reconstitutes
taxa after fusion), as well as the power of the ecological potential,
seems to be illustrated dramatically by the complex, mosaic interrelationships between two subspecies of the darter Etheostoma ( formerly
Boleosoma) nigrum in the Great Lakes and upper Mississippi regions. One form, E. n. nigrum, much the more widespread and
ubiquitous, inhabits chiefly terrigenous bottoms of open sand and
mud, whereas the other, E. n. eulepis, is more typical of vegetated
habitats. The open-water form, in apparent adaptation to its need
for very abrupt darts to avoid capture, is usually slenderer and has
rather smooth scales except on the head and adjacent regions, which
are largely scaleless. The other form, eulepis, is generally more robust
and has more strongly armed scales, which extend farther than
those of the open-water form in that they largely cover the nape,
breast, and cheek regions—suggesting that this roughness has adaptive value, probably in limiting predation by some small, though
significant, amount. Experiments by Lagler and Bailey ( 1947 ) show
that the differences are genetic. Each pattern of squamation has, we
may assume, some advantages and some disadvantages, but the advantages of smoothness seem to dominate on the more open bottoms,
while spininess seems to play the chief adaptive role in the more
vegetated habitats. In Glacial lakes that are predominantly free of
vegetation typical nigrum holds forth. A considerable number of lakes
that are well vegetated, scattered far and wide within the general
range of B. n. nigrum, harbor B. n. eulepis exclusively. Each subspecies, in waters that it exclusively occupies, tends to wander rather
freely into habitats characteristic of the other. Regions with varied
habitats and free passage, like the upper Mississippi River proper,
are occupied by intergrades, and probably have been so populated
through Postglacial time. During Postglacial redispersal the ancestors
of lake populations now occupied by the respective forms presumably
passed through and constituted part of this intergrade population. On
15
Comparative Isolating Mechanisms
their re-establishment in Glacial lakes, selection apparently reconstituted some into the eulepis type, others into the typical nigrum type.
Lake St. Clair, the adjacent Detroit River, and the western part of
Lake Erie now constitute a major and appropriate habitat of eulepis,
as they probably have through much of the time when, during Postglacial redispersal, populations of Boleosoma were funneled through
this area. On this assumption the individuals that moved on northward ( and the genes for vagility may be associated with those for
nigrum characters) became at once subject in the barren waters of
Lake Huron to adaptation for nigrum characters, which in time became reconstituted in the population. But where habitat conditions
favored the characters of eulepis, selection led toward, or to, that
form.
Resistance to swamping may be effective even within a single lake.
Thus, I found that two subspecies of Mollienisia mexicana occur in
the large Laguna de Peten in Guatemala. They are segregated ecologically or microgeographically. One form occupies the definite
marshy shallows; the other is semipelagic in the open waters ( to
which it is well adapted by its slender form, pale colors, and other
characters). Along the outer fringe of the marsh, between the habitats
of the two forms, I found a band of intergrades. The two forms freely
produce fertile offspring in aquaria. Since they do intergrade when
they come into contact in nature, one wonders why they have not
gradually amalgamated. Obviously some force has countered the
tendency to fuse. I interpret the force to be the effective adaptation of
each subspecies to its own habitat, so that a high breeding potential
is realized and the appropriate habitats are saturated with their respective pure stocks.
In still larger lakes, for example in Lake Nyasa, where essentially
sympatric speciation seems to have been rife, hybrids may be eliminated while the process of geographic and systematic divergence
progresses ( Fryer, 1959).
Some of these hypothetical speciational interplays may not have
been enacted in quite the way suggested, but there seems to be little
reason to doubt that differential selection has led to the build-up of
populations—such as those of Boleosoma n. nigrum, B. n. eulepis, and
intergrades—that have resisted the inflow of genes of other types,
perhaps by sheer reproductive potential and competition. Although
inherent genetic barriers to gene flow are few there has been no such
16
Isolating Mechanisms in the Speciation of Fishes
complete gene spread that many have insisted must eventuate wherever and whenever gene flow is made possible by topographic conditions and by the fertility of offspring. Opposing tendencies may be
stronger—and probably often are.
Must Segregation Be Geographic?
A major question is whether genetic isolation
can be accomplished without strict geographic segregation. The
Chairman has championed the view that it cannot and he has a wide
following. Perhaps I am a bit lonesome in disagreement. No one, of
course, doubts that geographic isolation is a major factor in speciation, and if one uses glasses with sufficiently high magnifying power,
even microhabitats or niches may be termed distinct geographic
entities.
But in practice we are dealing with more than semantics, as we
may see from two examples. The first concerns the plethora of cichlids in the great lakes of Africa. The usual view has been that this
abundance indicates multiple speciation in one body of water. Greenwood ( 1958 ), inspired by Mayr, interprets the events that led to such
profuse speciation as the formation, during the less pluvial periods,
of several very shallow lakes, in which populations became isolated
long enough to allow speciation to proceed to the level of mating incompatibility on the subsequent fusion of these ponds. The second
example concerns the chars in Windermere. Dr. Frost has interpreted
spring-spawning and fall-spawning stocks of chars in Windermere as
the product of speciation in situ, and the deep-water dwarf type she
has begun to study should fit into the same potential explanation. Dr.
Svardson, a distinguished disciple of the Chairman, has taken the
view that the seasonal races are distinct species that arose somewhere
else in geographic isolation, and independently reached Windermere
in their dispersal, and I suppose he would follow the same reasoning
for the deep-water dwarf.
These alternative explanations stand in bold contrast. For the
moment, at least, I do not see how we can submit either view to experimental test, nor have we unearthed as yet fossil records of sufficiently assured completeness to be critical. We are, however, not
totally lacking in pertinent indications.
Let us first consider the case of explosive evolution in lakes. To
me, Greenwood's explanation seems inherently implausible and
17
Comparative Isolating Mechanisms
forced. In general, shallow ponds are not scenes of extensive speciation, and we can hardly conceive that differentiation proceeded so
far in several such ponds in one lake basin as to have yielded the vast
diversity that exists in the lake today. Nor can we conceive its having
proceeded so far that fusion would not have occurred when the pond
segregates were brought together by the reunion of the ponds to form
Lake Victoria. No great diversity has arisen within small lakes and
ponds over Africa.
Can Greenwood's explanation be applied to other supposed scenes
of explosive lacustrine evolution? I doubt that Lake Tanganyika went
through a history of disruption and unification that would adequately
explain the numerous genera and the multitude of species that appear
to have arisen there from a very few ancestors. Fryer ( 1959 ) gave
cogent reasons why and how radiative adaptation has taken place
within Lake Nyasa. He presented very plausible models to illustrate
sympatric speciation in this lake.
It also seems unlikely that such a concept could explain the origin
in the Lake Lanao Basin in Mindanao of several genera and a considerable number of species of minnows from the single plausible
ancestor, Barbus ( or Puntius) binotatus ( Herre, 1933; Myers, 1959),
though here, as elsewhere, an effort should be made to reconstruct
the lake history by limnological and paleoclimatological data. In
Lake Lanao, as in the large African lakes, the explosive evolution has
gone to excessive extremes, nowhere attained outside these lakes
( Myers, 1960).
Comparable to the diversity of cichlids in African lakes is the diversity of the genus Orestias in Lake Titicaca ( Tchernavin, 1944). A
few rather ordinary species occur in other high Andean lakes, but the
great bulk of the species and all of the extreme variants occur only in
Lake Titicaca, just as the more extreme cichlids are confined to Lake
Tanganyika and other large African lakes, That they ever occurred
elsewhere seems to me inherently improbable.
Suggested Pathways for Essentially
Sympatric Speciation
The genetic segregation that is an essential
antecedent to speciation may be accomplished sympatrically by any
of a number of changes in the germ plasm that render some sets of
individuals interfertile among themselves but intersterile with other
18
Isolating Mechanisms in the Speciation of Fishes
individuals in the population—but it seems doubtful that such segregation has been at all common or effective among vertebrates.
Some degree of spatial or temporal segregation may be assumed.
The simplest form of such segregation is that of allopatry, which may
arise either through the dispersal of segregates of a population or
through such environmental modifications as stream capture; disruption of drainage systems; isolation of marine populations through
the closure of straits ( as by the elevation of the Isthmus of Panama);
antitropical separation through the warming of the tropics ( see, for
example, Hubbs, 1952); local survivals, for example on mountaintops
or in bogs, of populations that otherwise moved out of the region in
the course of Postglacial redispersal; separation on islands as a result
of elevations of the sea or of depressions of land masses; analogous
isolations on land through climatic or other changes that render uninhabitable a reticulum between habitable island-like remnants of
the former range. Such segregations have no doubt been frequent,
and very probably the usual, antecedents to differentiation. I know
of no serious student of speciation who questions that such enforced
regional segregations set the stage for differentiation which in due
course leads to genetic incompatibility.
Despite strong argumentation to the contrary, the possibilities of
essentially sympatric speciation pose a timely and worth-while problem for consideration. I insert the attributive "essentially" because I
am still thinking of assortive mating, within two or more groups of
individuals, induced to some degree by the close association of mating pairs. The question is in part one of semantics. That all degrees
of segregation exist—in terms of distance, time, and the amount of
interbreeding—is obvious. The question may be put in this way: did
the ecologically or temporally segregated and often adapted races
that occupy essentially the same area ( patria ) —or in the case of some
temporal segregates the identical habitat—originate in situ, or did
they first differentiate in areas that are definitely separated geographically, and then come into essential cohabitation after genetic isolation
had more or less developed? Some examples from fishes may be cited
to clarify the question: two races of salmon ( Oncorhynchus sp. )
that breed in adjacent tributaries; two types of trout (Sarno sp. )
that run into one stream to breed in successive periods; the two
shallow-water races of Salvelinus alpinus that breed at different times
on different shores of Windermere in England, as well as a deep19
Comparative Isolating Mechanisms
water race in the same lake ( data from Dr. Winifred Frost); normal
and neotenic types of smelt (Osmerus sp. ) that occupy the same
lake; three types of perch (Perca flavescens) that I observed in
Douglas Lake, Michigan—two in different parts of the main lake and
an extreme form in a marshy delta; shallow-water and deep-water
races of various fresh-water and marine fishes; littoral and pelagic
races of various marine fishes, or the marsh and open-water races of
Mollienisia mexicana in Laguna de Peten, referred to above; the bay,
littoral, and island subspecies of topsmelt ( Atherinops affinis) of the
Pacific Coast; ecologically segregated species of pipefish ( Syngnathus) in the same region; and ecosubspecies of cyprinid and other
fishes within one river system that are specifically adapted to different
current conditions. Examples could be multiplied ( and some might
need be deleted if the observed differences should prove to be wholly
phenotypic). I grant that it seldom will be possible on any present
evidence to answer these questions with full assurance, but the
weight of evidence seems to me to indicate that gradual speciation in situ, by increasing segregation, may often have been the
process.
That ecologically and temporally segregated fish taxa may often
have developed within single areas is strongly suggested by the varying degree of subspecific intergradation that often persists or of interspecific hybridization ( the distinction is often arbitrary—Hubbs,
1943). Thus the bay and ocean races of topsmelt (Atherinops affinis)
intergrade in the bay entrances, and in the intermediate stream
habitats of various fresh-water fishes there are intergrades, or even a
series of definable intergrading races, between the small, chunkybodied, large-scaled, fewer-rayed, smaller- and rounder-finned, deeppeduncled headwater types of pool-and-riffle habitats, on the one
hand, and, on-the other, the larger, slenderer, and finer-scaled types,
with larger and more falcate fins and a slender caudal peduncle, that
inhabit constantly swift creeks and rivers in the same stream system,
within which the populations are more or less continuously distributed ( Hubbs, 1941).
The initial step in segregation that may allow the gradual onset
of differentiation, particularly where selectional pressure is high, is
probably often provided by homing behavior, which has been found
to be highly developed in many fishes. Raciation is particularly well
marked in those fishes, such as the salmonids, in which homing is
20
Isolating Mechanisms in the Speciation of Fishes
most sharply developed; but both raciation and homing have been
demonstrated to be characteristic, to varying degrees, of many other
fishes of streams, lakes, and marine habitats. At first the homing is
often, and probably is typically, nongenetic, as it must be in transferred salmon stocks. Gradually, however, genetic responses involved
in the location of the spawning areas doubtless come into play, and
concurrently morphological differences develop. Increased segregation and increased adaptation are mutually advantageous and, therefore, subject to selection. In time, speciation may become complete.
As the segregated stocks become increasingly restricted to diverse
niches and increasingly specialized to the local conditions the high
breeding potential will undoubtedly produce large and distinctive
populations. Intergrades or hybrids will be outnumbered and will
tend to be overwhelmed by competition. It seems obvious that the
gradually lessened fecundity and viability characteristic of hybrids
will further reduce their numbers.That the pure stocks will more or
less completely replace the intermediates may be assumed, since even
small differences in selection are eventually effective.
Certain specialized habits, notably oral gestation in the cichlids,
apparently favor sympatric differentiation ( Fryer, 1959).
Summary
Speciation is visualized as a fluctuating conffict between the unifying effects of crossbreeding and the trend
toward genetic isolation. Intrinsic genetic mechanisms are involved in
genetic isolation, but extrinsic factors are often more important. Many
species that may be crossed readily by artificial fertilization or by
enforced cohabitation in aquaria seldom, if ever, hybridize in nature.
Behavioral and habitudinal factors are no doubt often effective.
Blocks to interbreeding develop in sympatry, but may be lost by isolated stocks within centuries. Hybridization often occurs when two
species or stocks previously separated are brought together in nature.
Unbalanced numbers favor hybridization, but other factors are involved. Disturbances of habitats, either natural or artificial, often lead
to crossbreeding. Some factors that lead to genetic isolation seem to.
be genetic; others, not. In general, with some minor exceptions,
genetic isolation increases with phyletic differentiation.
Various factors resist genetic swamping, even of closely approximated types. Prominent among these factors are the high breeding
21
Comparative Isolating Mechanisms
potential of the pure stocks, especially when well adapted to a particular environment. The intergrades or hybrids tend to be swamped
out by population pressure and competition, and are often reduced
by reason of some small degree of lowered viability or lowered fertility. Selection may continue to sort out genetic types, even after
fusion.
Although isolation is undoubtedly a common and probably the
usual antecedent of differentiation, segregation and speciation apparently may often be effected in essential sympatry. This seems to
be particularly true in lacustrine loci of explosive evolution. Homing
behavior, at first wholly or largely unfixed genetically, may be a prime
factor in sympatric speciation. Specialized habits, such as oral gestation, may well favor such differentiation.
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Isolating Mechanisms in the Speciation of Fishes
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23