19
SPECIES AND ALLOPATRIC
SPECIATION
Species are merely those strongly marked races or local forms
which, when in contact, do not intermix.
A.R. Wallace
Biological species is an evolving but stable group of
individuals arising and held together by a sensorily determined
common mating system, which isolates them reproductively from
any other group of individuals. On theoretical grounds, it is
plausible that geographic isolation, over time, as a result of
accumulation of phenotypic (morphological, physiological,
behavioral) differences, can lead to reproductive isolation of
populations and to allopatric speciation. However, the
terrestrial and aquatic environments on earth generally are too
continuous to account for the evolution of many millions of
extant metazoan species and an even greater number of extinct
species. The overwhelming majority of metazoan species evolved
in almost barrierless continents and oceans rather than in
isolated islands or lakes. Presently, it is difficult to assess
therelative role that geographic isolation and allopatric
speciation may have played in the evolution of metazoans. Models
of allopatric speciation fail to determine the mechanism of
reproductive isolation on secondary contact, when named species
that are potentially capable of producing viable and fertile
offspring do not interbreed and continue to exist as distinct
species in sympatry.
The Concept of Species
Darwin
considered species to be qualitatively not different from
varieties, and he used the term species for “the sake of
convenience” rather than for describing a taxonomic unit:
I look at the term species as one arbitrarily given, for the
sake of convenience, to a set of individuals closely resembling
each other, and that it does not essentially differ from the
term variety, which is given to less distinct and more
fluctuating forms. The term variety, again, in comparison with
mere individual differences, is also applied arbitrarily, for
convenience sake. (Darwin, 1859c)
The
post-Darwinian biology has generally recognized the real
existence of species as an evolutionarily discrete group of
individuals. However, Darwin’s concept contains an important
element of truth in the meaning that species, however discrete,
are evolutionarily transient states of supraindividual
organization and evolution of multicellular organisms.
In the
neoDarwinian era, species was universally recognized as the
fundamental taxonomic unit of evolution. One of the most widely
accepted concepts of species is the biological species concept (BSC)
introduced by Dobzhansky, who considered species to be
That stage in the evolutionary process
at which the once actually or potentially
interbreeding array of forms becomes segregated in two or more
separate arrays which are physiologically incapable of
interbreeding. (Dobzhansky, 1935)
The concept was later echoed and developed by
Mayr:
Species are groups of actually or potentially
interbreeding natural populations which are reproductively
isolated from other such groups. (Mayr, 1942)
At the core of the BSC is the notion of
reproductive isolation. BSC implies and proclaims that allopatry
is the necessary and sufficient condition of speciation.
Needless to say, Darwin did not relate speciation to allopatry.
The biological species concept, like about two
other dozens concepts of species, is far from universal as far
as its applicability to various forms of life is concerned. It
is not applicable to most unicellular prokaryotes, as well as to
a great number of asexual, parthenogenetically reproducing
invertebrates, self-pollinating plants, and many
interspecifically hybridizing plants.
Dobzhansky’s and Mayr’s definitions of species are inseparable
from the neoDarwinian assumption that geographic isolation is
the necessary and sufficient condition for the establishment of
reproductive isolation and speciation. This implies that
reproductive isolation of one species from another results from
accumulation of genetic changes between populations that have
been geographically isolated for long periods of time. At that
stage they represent species that are postzygotically isolated,
i.e. that even when secondarily come in contact and can
interbreed, they are incapable of producing fertile hybrids.
This prediction is not always validated by observations in
nature. Ever-increasing evidence, is showing that many
well-established vertebrate and invertebrate species are
reproductively not isolated, i.e. are “potentially
interbreeding” groups and their offspring gives birth to viable
and fertile offspring. This shows that the reproductive
incompatibility and post-zygotic isolation as criteria for
biological species definition are not universally true.
Later, due to inherent flaws of the definition and problems
arising from recognition of the BSC, numerous attempts have been
made to redefine the concept of species [24 named species
concepts were known until in 1997 (de Queiroz, 2005)].
It is not within the scope of this discussion to review
different species definitions still in wide currency in the
biological community. By emphasizing the role of reproductive
isolation in the process of speciation, the BSC underestimates
(while implying) the most important cohesive force of the
species, the mate recognition system, which represents the
deeper causal mechanism responsible for establishing
reproductive isolation between populations of the original
species. Reproductive isolation is determined by neurocognitive
mating decisions on the basis of mate preferences.
Observations on a number of morphologically and genetically
sibling (cryptic) species lends some weight to Paterson’s
recognition species concept (RSC), which, in distinction from
the BSC, views the reproductive compatibility within the
group, as a basic criterion of species definition.
Paterson’s recognition species concept maintains that
species is the most inclusive population of biparental organisms
sharing a common fertilization system. The concept emphasizes
the reproductive unity of the group, rather than its differences
with other groups. It emphasizes what reproductively the group
is rather than what it is not. The reproductive isolation
results from a change in the mate recognition system, which
creates “a common fertilization system” in a group of
individuals of a species.
The species recognition concept also is not applicable to
asexual organisms. Both RSC and BSC would deny the status of
species to many organisms that under natural conditions do not
hybridize but can hybridize and produce fertile hybrids under
special conditions.
In an attempt to overcome difficulties arising from almost all
the definitions that used to emphasize particular properties of
species for species definition, recently de Queiroz has proposed
another concept of species according to which the evolutionary
divergence between lineages leading to speciation first leads to
quantitative divergences between lineages, which over time may
produce distinctive character states. de Queiroz envisages
species formation as a process of continuous divergence of
populations that, over time, leads to sequential, but temporally
not orderly, acquisition of specific properties (phenetic
distinction, ecological distinction, changes in mate recognition
system, prezygotic isolation, postzygotic isolation, differences
between diverging lineages etc.) (de Queiroz, 2005; figure
19.1).
Figure 19.1.
A highly simplified representation of the process of
metapopulation lineage divergence (speciation) illustrating the
conflicts caused by adopting different contingent properties of
metapopulation lineages as necessary properties of species.
Progressive darkening and lightening of the daughter lineages
represent their progressive divergence through time (bottom to
top), and the numbered lines labeled SC (species criterion) 1–8
represent the times at which the daughter lineages acquire
different properties relative to one another (e.g., when they
become phenetically distinguishable, diagnosable by a fixed
character difference, reciprocally monophyletic, reproductively
incompatible, ecologically distinct, etc.). Before evolution of
the first property (SC1), authors will agree there is a single
species, and after evolution of the last property (SC8), they
will agree there are two. Between these events, however, there
will be disagreement among authors about whether one vs. two
species are involved. Those disagreements result from authors
adopting different contingent
properties (species criteria) as the basis for their
species definitions (From de Queiroz, 2005).
de Queiroz’s
species concept attempts to eliminate conflicts between various
species concepts, which are based on particular properties that
may appear at different stages of the process of speciation but it
fails to show when a separately evolving population should be
considered a true species. While attempting to reconcile widely
different definitions of species, this concept,
à la Darwin,
blurs the difference between varieties and species.
The speciation concept used in this work holds that reproductive
isolation may take place in sympatry and, in line with the
Darwinian concept of speciation. No geographic isolation or
post-zygotic isolation is required for reproductive isolation and
speciation process to take place. Reproductive isolation will be
considered as an initial step of speciation that relies on a
sensory determined ability of males and females to know, and with
a strong bias mate with self-like individuals, leading thus to
formation of two or more reproductively isolated populations
within the range of the original population. What prevents
hybridization and determines the reproductive isolation under
natural condition is the SMRS (specific mate recognition system).
In this work the
biological species will be dealt with as a transient but stable
group of individuals held together by a common mating system,
which under natural conditions determines their reproductive
isolation from individuals of the rest of mating systems.
A species, in
response to external/internal stimuli, can split into new mating
systems based on changes in mating preferences in groups of
individuals, and lead to formation of reproductively isolated
populations within the original population. Thus, the reproductive
isolation of two populations under conditions of sympatry, is
considered to be the result of the emergence of new mating
preferences in two groups of individuals of a single population,
which serve as cohesive forces for creating and maintaining two
new mating system. This form of reproductive isolation depends on
and derives from changes in the mating system. At the basis of the
sympatric speciation, thus, is an endogenously determined
reproductive isolation, as opposed to the exogenous reproductive
isolation imposed by spatial separation of populations (geographic
isolation) occurring during allopatric speciation.
While recognizing
the reproductive isolation both as a result and a condition of the
speciation process, this concept, in line with adequate
experimental evidence, rejects the “incompatibility of
interbreeding” as a criterion of speciation. Reflecting the
available empirical evidence it also rejects two neoDarwinian
tenets:
1. Genetic changes as cause of speciation,and
2. Postzygotic isolation as a criterion of species.
The NeoDarwinian Theory and the
Problem of Speciation
In developing his
theory of evolution via natural selection C. Darwin, for obvious
reasons, did not attempt to elaborate on the process of
speciation, the crux of the process of metazoan evolution. He
believed that speciation in plants and animals occurs in sympatry,
implying that no geographic isolation was necessary for the
process to take place.
After Darwin and
up to the present day the evolution of life has been considered to
be a gradual process of accumulation of heritable variations that,
over time, lead to reproductive postzygotic isolation of
populations and formation of new species. Accordingly, splitting
of one species in two is the unavoidable result of gradual
accumulation of variations, rather than an independent process of
evolution:
Speciation, then, is an epiphenomenon of Darwinism in only the
trivial sense that, like nearly all evolutionary phenomena, it
occurs by gradual change of populations, usually impelled by
natural selection. (Coyne, 1994)
This view has only rarely been challenged, despite the fact that
it has never been seriously attempted to theoretically elaborate
on the mechanism of speciation or experimentally trace back the
details of the process of accumulation of gradual changes, under
the action of natural selection, presumably leading to
reproductive isolation of populations.
However discrete, and obviously different from each other, species
were seen as demonstration of gradualism in the great scheme of
evolution of the living world. Nevertheless, the unmistakable
links and signs of transition between species and other higher
taxa in nature do not by themselves prove the belief that
accumulation of gradual hereditary changes is a mechanism, let
alone the only mechanism, of speciation.
Contrary to the mainstream of the biological thought, during the
last 140 years, a number of biologists, especially from the field
of paleontology, have continually challenged the gradualist
concept and presented evidence that seemed to contradict the view
of gradual speciation and evolution. But amid the unprecedented
enthusiasm engendered by the triumph of the classical and
molecular genetics and the advent of the neoDarwinian paradigm,
for the most part of the 20th century their claims
remained “voice in the desert”.
After de Vries’
saltationist theory of species formation, known as the mutational
theory, by 30s of the last century, the field of evolutionary
theory was dominated by the neoDarwinian thought. In the
neoDarwinian definition, essentially, evolution was a statistical
process of changes in allele frequencies, under the action of
natural selection. Constrained by the fact that genetic changes
that could occur in natural populations would be diluted under
conditions of panmixis, neoDarwinians had to postulate that
geographical isolation of evolving populations was a necessary
condition of speciation in nature, although Darwin envisaged
speciation as a process occurring in sympatry. Allopatric
populations, under the action of natural selection, accumulate
changes in the genotype, leading to their genetic divergence,
postzygotic and reproductive isolation and, finally, to formation
of new species. According to this allopatric model of speciation,
geographic isolation, the absence of physical contact between
populations, is an indispensable condition of speciation.
From the
neoDarwinian perspective, formation of new species and higher taxa,
the macroevolution in general, was seen as nothing more than an
extension, or an unavoidable finalization, of the process of
gradual accumulation of microevolutionary (mutational) changes in
genes. Accordingly, the difference between two processes lies not
in the mechanisms used, or in the causal basis, but in results
alone. And the difference in the results is a function of time.
Any ongoing microevolutionary process, at some point in time,
sooner or later, would produce macroevolutionary events. In a
well-known aphorism, microevolution plus sufficient time equals
macroevolution. Time only is necessary for macroevolutionary
events to occur, sufficient time for accumulation of
microevolutionary changes.
The neoDarwinian gradualistic concept of evolution took a serious
blow in early 70es, of the 20th century when two young
paleontologists, Niles Eldredge and Steven Jay Gould, based on
paleontological evidence, proposed their theory of punctuated
equilibria that evolution is characterized by long periods of
stasis (Eldredge, 1971) with no observable changes in morphology
and sudden, relatively short, periods of evolutionary changes (Eldredge
and Gould, 1972). They proposed that lack of transitional forms in
the paleontological record, was “an accurate reflection of
evolution” rather than result of the imperfect record (Gould,
1991). They argued that
Darwin had to emphasize the incremental, gradual character of
evolutionary changes in his confrontation with the prevailing
concept of the immutability and permanence of species. Says
Eldredge:
Gould and I showed that such stability is a real aspect of life’s
history which must be confronted - and that, in fact, it posed no
fundamental threat to the basic notion of evolution itself. For
that was Darwin’s problem: to establish the plausibility of the
very idea of evolution, Darwin felt that he had to undermine the
older (and ultimately biblically based) doctrine of species
fixity. Stasis, to Darwin, was an ugly inconvenience. ( Eldredge,
1985)
As Mayr pointed out, Darwin has been
Fully aware of highly different rates of evolution, from complete
stasis to rates of change so fast that intermediates could not be
discovered in the fossil record. (Mayr, 1992)
Indeed, in Darwin’s work, evolutionary gradualism is related with
the action of natural selection but the fact that Darwin himself
has repeatedly and explicitly stated that natural selection is not
the only mechanism of evolution (Darwin, 1859a1; Darwin, 1872a1)
indicates that he accepted the possibility of nongradual
evolution.
Beginning from the early 80es, studies of the Cambrian fauna
showed that about 540-570 Mya, within a short period of ~10
million years, all the known extant and many more extinct phyla
evolved with extraordinary and inexplicable rapidity. This
“Cambrian explosion” of metazoan life was a major blow to, and an
empirical refutation of, the neoDarwinian principle of gradualism
as the only way of evolution and speciation.
Since it was
first proposed in 30es of the last century, for more than 70
years, the neoDarwinian theory has been the prevailing theoretical
guide and inspiration for evolutionary studies in metazoans.
Tremendous amount of time and energy has been devoted to the
elaboration of hypotheses of gradual speciation through natural
selection acting as an editor on genetic variability that results
from spontaneous mutations, genetic drift, and gene flow.
It was taken for
granted that changes in genes are the only mechanism of induction
of inherited changes in the living world. While the role of
mutations in molecular evolution, i.e., in changing properties of
proteins is sufficiently and satisfactorily substantiated, it has
never been demonstrated that particular mutations in a gene or in
a number of genes have been responsible for an adaptive
morphological change in metazoans. Random mutations generally
produce “noise”, and very rarely can improve the functions of
proteins coded by genes but, to build on the neoDarwinian metaphor
of the of natural selection as the “editor” of the text of the
randomly occurring mutations, they produce no meaningful
(adaptive) morphological texts. Gene mutations, by definition,
produce changes in proteins by changing the amino acid sequence in
protein molecules, but it is beyond imagination how a change in
the amino acid sequence of a protein may change a morphological
character, that is an adaptive change in the spatial patterning of
millions/billions of cells of particular types from which the new
morphological character arises. This is the reason why no one has
ever attempted to hypothetically show, let alone elaborate on, how
this could happen.
By taking for
granted that changes in genes determine animal morphology, before
trying to show how this might occur, before demonstrating that
gene mutations and changes in allele frequencies are the real
cause of morphological variability, a whole mathematical structure
was created to show how these unproven genetic mechanisms drive
the evolution of living forms. On this scientifically shaky
foundation, the huge edifice of population genetics, the
mathematical basis of the neoDarwinian evolutionary theory, was
erected.
Adequate
experimental and observational evidence has already invalidated
the neoDarwinian tenet that geographic isolation, i.e. the spatial
separation of populations, under the action of natural selection,
is a necessary and sufficient condition of speciation. Allopatric
populations of a species commonly are capable to hybridize and
give birth to fertile offspring, which refutes the neoDarwinian
hypothesis of the evolution postzygotic isolation in allopatry as
a condition of speciation. Not only allopatric populations of a
species but, in some cases, named species belonging to the same
genus, and even to different genera, which have been
geographically separated for evolutionarily long periods of time
since they diverged from their common ancestor, are still capable
of hybridizing and producing fertile offspring in F1.
Empirical
evidence also shows that speciation does not necessarily require
long periods of time (for accumulation of “favorable mutations”)
to occur. Species are known to have evolved in “evolutionary
instants” of a few thousands (cichlid fushes in East African
lakes) and even a few hundreds (Rhagoletis spp.) of years.
None of the
neoDarwinian agents of evolution (gene mutations, genetic
recombination and changes in allele frequencies) have been
demonstrated to affect speciation events in sympatry or allopatry
and often sibling species are both morphogenetically and
genetically almost indistinguishable (Purves and Orians, 1987a).
Sometimes, sibling species that are reproductively isolated show
no genetic differences and often, genetic differences between
individuals and populations of the same Drosophila species
are greater than those between sibling species:
Gel electrophoretic techniques reveal that sibling species of
Drosophila share nearly all their alleles. The prevalent
allele at most loci is nearly always found at a frequency of at
least 0.01 in other closely related species. The vast majority of
differences among the species is based upon variability already
present within the individuals of a species. All of several
hundred species of this genus that have evolved in Hawaii during
the past 5-6 million years are very similar morphologically
and genetically. (Purves and Orians, 1987b)
This is also the case with other invertebrate taxa:
The genetic variation among the 200 Lake Victoria species is less
than that within a single species of horseshoe crab; and yet the
morphological variation among them is extensive. (Levin, 1999)
Under drastically
changed conditions of living, speciation may occur very fast,
within a limited number of generations or in a few thousand years.
This has been the case with sympatric species of cichlid fish in
East African lakes, Drosophila species in Hawai islands,
etc. All these speciation events have taken place in the absence
of geographical isolation. From a neoDarwinian view, this is
inexplicable.
Formation of an
estimated 500 extant and extinct species of cichlid fish, of which
200 are endemic (not found elsewhere), in LakeVictoria within
750,000 years (Seehausen et al., 1997) is a stumbling block to any
attempt to explain it from the view of populations genetics and
the knowledge on mutagenesis in general.
Similarly, there
is no satisfactory neoDarwinian explanation of the exceptionally
rapid, linear evolution of hominids from Australopithecines living
some 4 million years ago through Homo habilis (3 million
years), Homo erectus (1.7 million years), Homo
neanderthalensis (400 thousand years), and Homo sapiens
sapiens (Cro-Magnon man) (~30 thousand years ago). The
sequential emergence of those ancestors of the Homo sapiens
sapiens could not reasonably be attributed to any form of
geographic isolation for the Old World represents a territorial
continuum, and the number of generations (a few thousands) is
obviously insufficient for the favorable changes to occur and
accumulate to the point of a genetic isolation and emergence of a
new species of strongly distinct phenotypes even under conditions
of geographic isolation.
The fact that
numerous demonstrated cases of speciation have occurred not only
within evolutionarily very short periods of time but also under
conditions of sympatry, clearly suggests that the neoDarwinian
principles of allopatry and gradualism are not validated as
scientific hypotheses for explaining the process of speciation.
These facts
suggest that genetic changes may not be related to, or be
necessary for, prezygotic reproductive isolation. It is possible
that the opposite might be true, i.e. that speciation may be the
cause of the accumulation of genetic and chromosomal changes
observed between species in sympatry and allopatry.
And the question
naturally arises whether that minimal amount of genetic and
morphologic difference between those species (which often is
smaller than the variability already present within the species)
is prespeciational or postspeciational by origin. We
have no reliable way of determining whether the genetic changes
between two extant species have occurred in allopatry or sympatry,
or before the speciation or thereafter, hence we are unable to
determine whether the two species evolved in sympatry or allopatry.
From a
morphological point of view, it is within everyone’s realm of
experience that various races of domestic animals, created through
artificial selection by man during last few millenia, are often
more different between them than from their wild conspecifics.
Very often, even under natural conditions, various races of a
species in sympatry differ so much phenotypically from each other
that for long periods of time have been viewed as distinct
species. This has been the case with the deer mouse (Peromyscus
maniculatus), the most widely distributed small animal in
North America, which exhibits extraordinary regional variations in
coat color, which matches the background color of soils, and in
tail and foot length, which determines how readily the deer mice
can climb (Purves, 1987c).
Speciation Modes According to the
Spatial Occurrence
Darwin adopted a sympatric approach to the problem of speciation
but post-Darwinian evolutionists distinguished between two main
forms of speciation, allopatric speciation, taking place under
conditions of spatial isolation of populations, and sympatric
speciation occurring within populations sharing the same habitat.
However, in line with the basic neoDarwinian tenet of accumulation
of changes in genes and alleles as a condition of speciation,
their approach required spatial isolation, for under conditions of
sympatry, the panmixis, random mating would not allow accumulation
of genetic differences between two populations. Hence, from a
neoDarwinian view, sympatric speciation is not more than a
theoretical possibility.
The classification of modes of speciation according to spatial
occurrence is a phenomenological classification, for the same
causes of speciation may be involved in both allopatry and
sympatry. However, for historical reasons and for facilitating the
argument, the following discussion on speciation will follow that
classification.
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