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Adaptation and The Origin of Species.
Author(s): Douglas W. Schemske
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Source: The American Naturalist, Vol. 176, No. S1, Darwinian Thinking: 150 Years after The
Origin A Symposium Organized by Douglas W. Schemske (December 2010), pp. S4-S25
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vol. 176, supplement
the american naturalist
december 2010

Adaptation and The Origin of Species
Douglas W. Schemske*
Department of Plant Biology and W. K. Kellogg Biological Station, Michigan State University, East Lansing, Michigan 48824
Online enhancements: appendix tables.
abstract: As reflected in the title of his masterwork On the Origin
of Species, Darwin proposed that adaptation is the primary mechanism of speciation. On this, Darwin was criticized for his neglect of
reproductive isolation, his lack of appreciation for the role of geographic barriers, his failure to distinguish varieties from species, and
his typological species concept. Two developments since Darwin, the
biological species concept of Ernst Mayr and the methods of Coyne
and Orr for estimating the contribution of different barriers to the
total reproductive isolation, provide a framework for reconciling Darwin’s view on the primacy of adaptation in speciation with later
proposals that emphasize reproductive isolation. A review of the few
studies that have estimated the contributions of multiple isolating
barriers suggests that habitat isolation and other barriers that operate
before hybrid formation are much stronger than intrinsic postzygotic
isolation. In light of these data, I suggest that Darwin’s focus on
adaptation in the origin of species was essentially correct, a conclusion that calls for future studies that explore the links between adaptation and speciation, in particular, ecogeographic isolating barriers that result from adaptive divergence in habitat use. The recent
revival in thinking about ecological factors and adaptive divergence
in the origin of species echoes Darwin’s much-criticized “principle
of divergence” and suggests that the emerging views from today’s
naturalists are not so different from those espoused by Darwin some
150 years ago.
Keywords: adaptation, Darwin, isolating barriers, reproductive isolation, speciation.
Introduction
According to my view, varieties are species in the presence of
formation, or are, as I have called them, incipient species.
How, then, does the lesser difference between varieties become
augmented into the greater difference between species? (Darwin 1859, p. 111)
Since the first publication in 1859 of Charles Darwin’s On
the Origin of Species, the topic of speciation has been the
subject of great interest and debate. The major problem
of speciation, succinctly expressed by Darwin above, is to
* E-mail: [email protected].
Am. Nat. 2010. Vol. 176, pp. S4–S25. 䉷 2010 by The University of Chicago.
0003-0147/2010/176S1-52252$15.00. All rights reserved.
DOI: 10.1086/657060
identify the ecological and evolutionary mechanisms that
cause populations to achieve the minimum level of divergence required for their classification as full species.
This requires answers to several challenging questions:
What criteria distinguish species from varieties? Can species arise within populations without extrinsic barriers?
What are the primary factors that contribute to the origin
of species?
To Darwin, the processes responsible for the origin of
species were essentially the same as those for the origin
of adaptations. Invoking his theory of natural selection,
Darwin reasoned that adaptation to distinct habitats
caused populations to diverge in ecologically relevant traits
and that the degree of morphological differentiation
among populations was the primary criterion for species
status. Much has been written about Darwin’s views on
speciation, largely focused on Darwin’s shortcomings. For
example, it has been suggested that Darwin’s typological
species concept, where species are diagnosed largely by
their morphological characteristics, is too subjective (Mayr
1992; Futuyma 1998). Darwin has also been criticized for
failing to acknowledge the role of geographic barriers in
the divergence of populations (Mayr 1959, 1992, 1994).
As discussed recently by Mallet (2008), these and other
considerations have led to the conclusion by many that
Darwin’s On the Origin of Species contributed little to solving the problem of speciation. In criticizing Darwin’s principle of divergence as an explanation for the origin of
species, Mayr (1942, p. 147) states, “It is thus quite true,
as several recent authors have indicated, that Darwin’s
book was misnamed, because it is a book on evolutionary
changes in general and the factors that control them (selection, and so forth), but not a treatise on the origin of
species. Obviously it was impossible to write such a work
in 1859, because the whole concept of the species was too
vague at that time.” Similarly, Coyne (1992, p. 511) suggested, “Despite its title, On the Origin of Species made few
inroads on this problem,” and Coyne and Orr (2004, p.
9) assert that Darwin’s perspective on speciation in The
Origin “is seen by most modern evolutionists as muddled
or wrong.” Noor and Feder (2006, p. 852) suggest that
“Darwin had only vague insights into the speciation pro-
Adaptation and The Origin
cess itself, viewing it as a later stage in a continuum from
adaptive divergence among ‘varieties’ within species.”
How could the same person who made the most significant contribution in the history of evolutionary biology, that is, the theory of natural selection, utterly fail to
appreciate species and speciation? Did Darwin overreach
in giving The Origin its title? I agree with Reznick (2010,
p. 137), who concluded “that Darwin did, in fact, write a
book about speciation.” Given Darwin’s protracted deliberations as he prepared his notes for publication (see below), it would be surprising if he had misrepresented one
of the focal points of his life’s work.
On this 150th anniversary of the publication of Darwin’s
seminal achievement, I discuss how his views on species
and speciation compare to those that have emerged since
The Origin. My main theme is the relationship between
adaptation and speciation. I attempt to reconcile Darwin’s
proposal that ecological differentiation is the primary
mechanism of speciation with the neo-Darwinian emphasis on the evolution of reproductive isolating factors. Despite many claims to the contrary, I suggest that these two
perspectives are essentially one and the same.
I begin with a historical treatment of how The Origin
came to be and then consider Darwin’s work on species
and speciation and summarize recent studies that investigate the relative importance of different isolating barriers.
I conclude that Darwin’s view of ecological differentiation
as the major factor in speciation is essentially correct. Nevertheless, further research is needed in a number of areas,
and these are outlined in the concluding remarks.
On the Origin of The Origin
To understand the development of Darwin’s views on natural selection and speciation, it is important to recognize
that The Origin was not the treatise that Darwin had
planned (Stauffer 1975). Instead, it was a hurriedly prepared “abstract,” written on the heels of his communications with Alfred Russel Wallace, who in 1858 surprised
Darwin with a letter outlining his independent discovery
of the principle of natural selection. The remarkable circumstances that led to the publication of The Origin are
summarized below.
After his five-year journey around the world on the
HMS Beagle (1831–1836), Darwin returned to England to
transcribe his notes and deliberate on his discoveries. Progress was slow. Darwin wrote early drafts of his ideas on
evolution in 1842 and 1844, but these were published only
after his death, by his son Sir Frances Darwin (Darwin
1909). With financial security, Darwin was free to explore
his many related interests. Before the publication of The
Origin, Darwin published well-known books on coral reefs
(1842) and volcanic islands (1844) based on observations
S5
he made while on board the Beagle, as well as two monographs on the taxonomy of barnacles (1851, 1854).
Describing his plan in a letter to William Darwin Fox
in 1855, Darwin wrote, “I am hard at work at my notes
collecting and comparing them, in order in some two or
three years to write a book with all the facts and arguments,
which I can collect, for and versus the immutability of
species” (Stauffer 1975, p. 5). Many of Darwin’s associates
encouraged him in this effort, with geologist Charles Lyell
playing a key role. In 1856, Darwin wrote to Lyell, “I have
found it quite impossible to publish any preliminary essay
or sketch; but I am doing my work as completely as my
present materials allow without waiting to perfect them.
And this much acceleration I owe to you” (Stauffer 1975,
p. 9).
Later that year, Darwin wrote to Lyell, “I am working
very steadily at my big book” (Stauffer 1975, p. 9). His
goal was never reached. Darwin had completed 10 chapters
for Natural Selection, his “big book,” when, on June 18,
1858, he received a letter from the naturalist Alfred Russel
Wallace describing views on evolution that were remarkably similar to his own. This led to the famous communication of their ideas to the Linnean Society later that
year (Darwin and Wallace 1858). In January of 1859, Darwin wrote to Wallace, “I look at my own career as nearly
run out. If I can publish my Abstract and perhaps my
greater work on same subject, I shall look at my course
as done” (Darwin 1887, 2:146–147). Darwin’s On the Origin of Species was published shortly thereafter, on November 24, 1859.
In addition to this “abstract” from Natural Selection,
Darwin also published The Variation of Animals and Plants
under Domestication (1868), which represents the first section of his manuscript. Darwin never published Natural
Selection, but a version edited by the historian Robert C.
Stauffer was published in 1975, under the title Charles
Darwin’s Natural Selection: Being the Second Part of His
Big Species Book Written from 1856 to 1858 (Stauffer 1975).
This invaluable resource is the result of Stauffer’s careful
and painstaking transcription of more than 1,000 pages of
Darwin’s largely illegible handwriting. As stated by Mayr
(1992, p. 343), in Natural Selection, “Darwin presented his
reasoning and his evidence in far greater detail than in the
Origin of Species. This permits a new and indeed more
definitive analysis.” Nevertheless, it is largely unappreciated that the ideas and examples presented in The Origin
often differ substantially from those in his unpublished
manuscript.
My references to Darwin’s On the Origin of Species, hereafter The Origin, are primarily from the first edition (Darwin 1859), which, with all other editions, is available online
at http://darwin-online.org.uk/. Reference to material in
S6 The American Naturalist
Natural Selection is from Darwin’s unpublished “big
book,” as transcribed by Stauffer (1975).
Species and Speciation
With the historical context of Darwin’s work as background, I discuss three core aspects of his theory on the
origin of species that continue to be debated today: (1)
the relationship between adaptation and speciation, (2)
the importance of geographic barriers, and (3) species concepts. To this end, I contrast Darwin’s views on these
topics, drawing on his writings in The Origin and Natural
Selection, with post-Darwinian perspectives. Any attempt
to characterize Darwin’s views is fraught with difficulty.
This challenge is illustrated by the following quote, communicated to James Mallet by one of his colleagues,
“Sometimes I think that Darwin, at least on speciation, is
like the Bible: one can buttress any view by choosing the
right quotation” (Mallet 2008, p. 4). While I too am not
immune to seeing in Darwin what I wish to see, I have
tried here to characterize accurately the various sides of
the controversies.
The Relationship between Adaptation and Speciation
Darwin more and more treated speciation as a process of
adaptation, an aspect of the principle of divergence, completely
omitting any reference to the need for the acquisition of reproductive isolation. (Mayr 1982, p. 416)
If one adopted Darwin’s claim, then the problem of the origin
of new species was virtually solved; every variety was at the
threshold of becoming a new species, and it required only a
little push of natural selection to complete the process. (Mayr
1992, p. 349)
For Darwin, the origin of species was identical to the origin
of adaptations within species—the production of different varieties. He therefore conflated the problem of change within
a lineage with the problem of the origin of new lineages.
(Coyne and Orr 2004, p. 11)
Mayr and others have criticized Darwin for not making a
distinction between adaptation and speciation, yet these
two evolutionary mechanisms are inextricably linked
(Schemske 2000; Schluter 2001, 2009; Rundle and Nosil
2005; Sobel et al. 2010). The closest Darwin came to making that association is laid out in his principle of divergence, the foundation of Darwin’s views on the origin of
species (Browne 1980; Mayr 1992; Pfennig and Pfennig
2010, in this issue). His argument is that adaptation and
natural selection cause varieties to diverge for ecological
and morphological traits that contribute to their competitive performance and that ultimately these heritable dif-
ferences are sufficient to elevate varieties to the level of
species. As Pfennig and Pfennig (2010) describe, Darwin’s
principle of divergence has implications for a number of
problems concerning the relationships between adaptation
and speciation, particularly the importance of character
displacement in adaptive divergence.
In chapter 4 of The Origin, Darwin (1859, pp. 127–128)
summarized his principle of divergence as follows: “Natural
selection, also, leads to divergence of character; for more
living beings can be supported on the same area the more
they diverge in structure, habits, and constitution. … Thus
the small differences distinguishing varieties of the same
species, will steadily tend to increase till they come to equal
the greater differences between species of the same genus,
or even of distinct genera.” In this same chapter, Darwin
describes a theoretical scenario for the evolution of varieties and species by his principle of divergence. Interestingly, this section includes the only figure in The Origin,
which, Darwin (1859, p. 116) states, “will aid us in understanding this rather perplexing subject.” The figure depicts evolution in a single large genus of organisms over
the course of 14,000 generations. The assemblage consists
initially of 11 species (A, B, …, L) that ultimately produce
15 descendant species: one of the ancestors (A) gives rise
to eight new species, another (I) gives rise to six new
species, and a third (F) gives rise to just one new species.
None of the other eight ancestral species produces any
living descendants. Darwin (1859, p. 120) states, “The diagram illustrates the steps by which the small differences
distinguishing varieties are increased into the larger differences distinguishing species.”
In Natural Selection, the principle of divergence is illustrated in detail, here for a hypothetical genus of plants
initially consisting of 12 species that differ in their moisture
requirements. Darwin states (Natural Selection [Stauffer
1975], p. 238), “The complex action of these several principles, namely, natural selection, divergence & extinction,
may be best, yet imperfectly, illustrated by the following
Diagram, printed on a folded sheet of paper for convenience of reference. This diagram will show the manner,
in which I believe species descend from each other & therefore shall be explained in detail.”
In this diagram, reprinted here (fig. 1), Darwin proposes
that the most “moisture-loving” species (A) gives rise to
three new species (a10, h10, and I10; superscripts denote
stages of descent) while the least moisture-loving species
(M) gives rise to one new species (m10). The new species
derived from species A are proposed to occupy a wider
range of conditions than those occupied by their ancestor,
“so that in love of moisture & in many other respects,
a1–10, h1–10, I1–10 would come to differ or diverge more &
more from each other & their original parent-stock” (Natural Selection [Stauffer 1975], p. 243). Likewise, Darwin
Adaptation and The Origin
S7
Figure 1: Diagram I from Darwin’s Natural Selection, illustrating the “Principle of Divergence” for a hypothetical genus of plants that differ in their
moisture requirements. The most “moisture-loving” species (A) gives rise to three new species (a10, h10, and I10; superscripts denote stages of descent),
one of which (a10) is more aquatic than its ancestor, and the least “moisture-loving” species (M) gives rise to one new species (m10), which is more
drought tolerant than its ancestor. The genus thus expands from 12 to 14 species that occupy a wider range of soil moisture environments than
their ancestors (reprinted from Stauffer 1975 with the permission of Cambridge University Press).
proposes that the new species m10 is more drought tolerant
than its ancestor (M). The other 10 original species persist
but leave no new descendants, and the original species A
and M are “supplanted” by their descendants. Thus, “the
genus will have become not only more divergent in character (a10 more aquatic than A; & m10 more droughtenduring than M) but numerically larger” (Natural Selection [Stauffer 1975], pp. 244–245), expanding from 12 to
14 species (fig. 1). It is worth noting that Darwin does not
explain here whether adaptive divergence is prompted by
a change in the environment or, instead, competitive interactions favor the partitioning of shared features in the
current environment.
In Natural Selection, Darwin summarized his views on
how natural selection leads to adaptively differentiated varieties and species:
A little reflexion will show the extreme importance of this
principle of divergence for our theory. I believe all the species
of the same genus have descended from a common parent;
& we may call the average amount of difference between the
species, x; but if we look at the contemporaneous varieties of
any one species, the amount of difference between them is
comparatively extremely slight & may be called a. How thus
can the slight difference a be augmented into the greater difference x; which must on our theory be continually occurring
in nature, if varieties are converted into good species? The
process feebly illustrated in our diagram, I believe, explains
this; namely the continued natural selection or preservation
of those varieties, which diverge most in all sorts of respects
from their parent-type. (Stauffer 1975, p. 243)
Darwin was criticized for failing to understand the distinction between adaptation and speciation. Here he makes
it clear that these subjects are inseparable.
Speciation and Geographic Barriers
Darwin’s basic oversight was that he failed to partition isolation into extrinsic geographical-ecological barriers and intrinsic isolating mechanisms. (Mayr 1982, p. 414)
Darwin established the principle of divergence in order to
substantiate a theory of sympatric speciation. (Mayr 1994, p.
529)
The idea of sympatric speciation was, of course, Darwin’s.
(Coyne and Orr 2004, p. 125)
The prevailing opinion among many evolutionary biologists is that Darwin believed that species could often arise
within populations without geographic isolation, that is,
via sympatric speciation (Mayr 1992, 1994; Coyne and Orr
S8 The American Naturalist
2004). Understanding Darwin’s position on the role of
geographic isolation in speciation is challenging. In discussing this point, Mayr (1994, p. 529) stated that in The
Origin, Darwin “omitted most of his putative evidence and
condensed his argument to such an extent that it is almost
impossible to follow his reasoning.” In addition, Darwin’s
views on isolation changed over the years, being influenced
by his efforts to understand the nature of inheritance (Vorzimmer 1965), by the development of his principle of divergence (see above), and through communications with
colleagues and critics (Sulloway 1979; Mayr 1982).
Nevertheless, Darwin did voice substantial support for
the idea that geographic isolation is often an important
factor in speciation. For example, in a letter to J. D. Hooker
in 1844, Darwin writes, “The conclusion, which I have
come at is, that those areas, in which species are the most
numerous, have oftenest been divided and isolated from
other areas, united and again divided; a process implying
antiquity and some changes in the external conditions.
This will justly sound very hypothetical. I cannot give my
reasons in detail; but the most general conclusion, which
the geographical distribution of all organic beings, appears
to me to indicate, is that isolation is the chief concomitant
or cause of the appearance of new forms (I well know
there are some staring exceptions)” (Darwin 1887, 2:28).
In The Origin, Darwin (1859, p. 105) suggested that
geographic isolation was important but not the main factor
in speciation, stating, “Although I do not doubt that isolation is of considerable importance in the production of
new species, on the whole I am inclined to believe that
largeness of area is of more importance, more especially
in the production of species, which will prove capable of
enduring for a long period, and of spreading widely.” From
this and other statements in this section, it appears that
Darwin is mainly speaking to how “largeness of area”
might provide increased opportunities for incipient species
to come into contact and therefore compete for similar
resources. Natural selection might then favor the evolution
of traits that increase competitive ability, that is, divergence
of character (Pfennig and Pfennig 2010), leading to speciation. In this regard, Darwin (1859, p. 106) states, “Each
new form, also, as soon as it has been much improved,
will be able to spread over the open and continuous area,
and will thus come into competition with many others.”
To emphasize that geographic isolation contributes to this
process, Darwin suggests (p. 106), “Moreover, great areas,
though now continuous, owing to oscillations of level, will
often have recently existed in a broken condition, so that
the good effects of isolation will generally, to a certain
extent, have concurred.”
Darwin’s clearest statements on the role of geographic
isolation are found in Natural Selection (Stauffer 1975),
for example, “I am inclined to believe, that wherever very
many individuals of a freely crossing & highly locomotive
animal existed, the retardation of any selected modification
from crossing would be so strong, that it could hardly be
overcome, without indeed the tendency to vary in some
particular direction was extremely strong. Hence I infer
that some degree of isolation would generally be almost
indispensable” (p. 255). Darwin notes that in birds and
mammals, varieties and the most similar species “generally
inhabit distinct areas” (p. 256). This is a prescient description of geographic speciation, and it portends the later
observation by Jordan (1905) that the most closely related
species typically have abutting distributions, as would be
expected if they arose in allopatry (Barraclough and Vogler
2000). Furthermore, Darwin recognized that in more sedentary organisms or those, like plants, that rely less on
cross-fertilization, divergence could proceed without complete isolation, “though in such cases, isolation, at least
partial isolation at first, would be favourable to their natural selection” (Natural Selection [Stauffer 1975], p. 256).
In 1876, responding to criticism from Moritz Wagner
that he had neglected to appreciate the role of geographic
isolation, Darwin stated, “I do not believe that one species
will give birth to two or more new species, as long as they
are mingled together within the same district. Nevertheless
I cannot doubt that many new species have been simultaneously developed within the same large continental
area; and in my ‘Origin of Species’ I endeavoured to explain how two new species might be developed, although
they met and intermingled on the borders of their range.
It would be a strange fact if I had overlooked the importance of isolation, seeing that it was such cases as that of
the Galapagos Archipelago, which chiefly led me to study
the origin of species” (Darwin 1887, 3:159).
The evolution of species from varieties by the process
of natural selection in Darwin’s description of speciation
seems perfectly consistent with the idea that geographically
isolated populations may incrementally acquire reproductive isolating barriers during adaptive divergence. Although Mayr (1992) criticized Darwin for not appreciating
the important of geographic barriers in speciation, in his
paper titled “Ecological Factors in Speciation,” Mayr
(1947, p. 263) states, “It appears to me that there is no
real conflict between those authors who stress the ecological aspects of speciation … and those, who, like myself,
have stressed geographical aspects.” He suggests that those
who emphasize ecological factors in the origin of species
“generally accept sympatric speciation as an integral part
of ecological speciation” (Mayr 1947, p. 263). Although
that is indeed a common view, there is no reason to invoke
sympatric speciation whenever ecological factors are
thought to play a primary role in speciation. Indeed, Coyne
and Orr (2004, p. 179), staunch advocates of the primacy
of allopatric speciation, state that “virtually all barriers can
Adaptation and The Origin
be considered ecological in the sense that they may arise
from environmentally imposed selection.”
Darwin clearly believed that under some circumstances,
divergent natural selection could occur between varieties
that are at least partially sympatric, perhaps elevating them
to species by divergent natural selection (Pfennig and Pfennig 2010). Yet I can find no evidence that Darwin believed
that varieties arise in sympatry and/or that species typically
evolve from sympatric varieties, as his critics have sometimes charged. As Sulloway (1979, p. 48) concluded, “without some form of isolation—whether complete, partial, or
behavioral—Darwin fully understood, and repeatedly insisted, that speciation would be impossible.”
Species Concepts
A species, as we now see it, is characterized not only by being
different, but also by being distinct from other species (separated by a gap, reinforced by isolating mechanisms). In his
more nominalistic treatment of species in the late 1850s Darwin was concerned only with difference, the first criterion of
this dual characterization. (Mayr 1992, p. 349)
In The Origin, Darwin apparently felt that species were not
real. (Coyne and Orr 2004, p. 10)
Part of the challenge in studying speciation is to develop
and implement criteria for distinguishing “species” from
other categories, such as varieties, subspecies, races, and
ecotypes. This is rarely a problem in sympatric taxa because
the maintenance of morphological and genetic differences
other than simple genetic polymorphisms is clear evidence
that sympatric populations function as distinct species.
The main problem is with allopatric taxa: are the observed
genetic/and or morphological differences sufficient to regard populations as distinct species? Darwin (1859, p. 52)
was unable to provide clear guidelines in these situations:
“It will be seen that 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.” It is understandable that this unambiguous statement is used to support the suggestion by many authors that Darwin saw no
difference between varieties and species and hence was
unable to make any real contribution to our understanding
of the origin of species (Mayr 1959, 1992, 1994; Futuyma
1998; Coyne and Orr 2004).
Yet, later, in discussing species of large genera, Darwin
(1859, pp. 57–58) reaches a different conclusion, stating,
“the amount of difference between varieties, when compared with each other or with their parent-species, is much
less than that between the species of the same genus. But
S9
when we come to discuss the principle, as I call it, of
Divergence of Character, we shall see how this may be
explained, and how the lesser difference between varieties
will tend to increase into the greater differences between
species.” It thus seems that Darwin recognized the importance of species in both evolutionary and taxonomic
terms. He spent years carefully studying the taxonomy of
barnacles, and Mayr (1992, p. 347) describes Darwin’s
travails in trying to assign species status in these organisms,
“I have gnashed my teeth, cursed species, & asked what
sin I had committed to be so punished.” Would Darwin
have engaged in these studies if he had no appreciation
for species?
Darwin also devoted a long section in The Origin to the
difficulties that he and other naturalists had in attempting
to distinguish species from varieties (chap. 2, the section
titled “Doubtful Species”). As one example, he refers to
the difficulties presented by the wide variability seen in
oaks. It is worth noting that using morphological traits to
delimit species boundaries in difficult groups like oaks
remained a challenge long after Darwin’s observation
(Burger 1975; Van Valen 1976), and it has taken new and
sophisticated molecular genetic approaches to resolve taxonomic and evolutionary questions in this group (Howard
et al. 1997; Dodd and Afzal-Rafi 2004; Lexer et al. 2006).
We now recognize that Darwin’s taxonomic struggles to
classify species were not simply a consequence of subtleties
in distinguishing “good” species. If speciation is the gradual accumulation of genetic, ecological, and morphological
differences, we should sometimes find intermediate stages
in speciation where closely related groups are substantially
differentiated but are not yet species (Grant 1957; Hendry
2009). As Grant (1957, p. 75) concluded, “Where species
originate from races by a continuous and gradual process
of evolution, some populations at any given instant will
be in a halfway stage between race and species.” It seems
that Darwin recognized this intermediate stage in speciation, hence his difficulties in drawing a clear line between
species and varieties.
Darwin also recognized that whether crosses between
varieties or putative species could create fertile hybrids was
a poor criterion for assigning species status. As discussed
by Mayr (1992, p. 353), Darwin’s perspective on this topic
was apparently influenced by his conversations with botanists, who recognized that many “good” plant species
could hybridize, “They convinced him … that sterility was
not the secure species criterion he had once thought.” In
Natural Selection (Stauffer 1975, p. 97), Darwin states,
“there are great difficulties … in taking lesser fertility in
the offspring as an unerring guide what forms to call species.” Darwin’s views were echoed by Huxley (1859, p. 8)
in his commentary on The Origin:
S10 The American Naturalist
But is it not possible to apply a test whereby a true species
may be known from a mere variety? Is there no criterion of
species? Great authorities affirm that there is—that the unions
of members of the same species are always fertile, while those
of distinct species are either sterile, or their offspring, called
hybrids, are so. It is affirmed not only that this is an experimental fact, but that it is a provision for the preservation of
the purity of species. Such a criterion as this would be invaluable; but, unfortunately, not only is it not obvious how
to apply it in the great majority of cases in which its aid is
needed, but its general validity is stoutly denied.
trinsic or intrinsic factors (Cronquist 1978). The same can
be said of species concepts based on phylogenetic differences: the criterion of “fixed diagnosable differences” for
diagnosis of species under the phylogenetic species concept
(Cracraft 1989) can be met only if there is a barrier to
gene flow between groups. Thus, Darwin’s approach to
the problem of species, that is, a search for biologically
meaningful discontinuities between groups, is not so different from current taxonomic practices.
The importance of hybrid sterility in the study of species
and speciation is still a matter of debate. For example, in
discussing Darwin’s rejection of hybrid sterility as a criterion for species status, Mallet (2008) applies a narrow
definition of reproductive isolation, treating intrinsic postzygotic isolating mechanisms such as hybrid sterility and
inviability as being the exclusive forms of reproductive
isolation. He suggests that “it is sufficient to say here that
we now know that a great deal of the evolution of reproductive isolation has nothing to do with speciation; instead
it occurs long after speciation has occurred” (Mallet 2008,
p. 12). The implication is that reproductive isolation is
synonymous with hybrid sterility and inviability and that
Darwin was right to reject reproductive isolation as a criterion for species. What Darwin really said is that given
the wide variation observed in the success of crosses between species, hybrid inviability and sterility are not sufficient in their own right to distinguish varieties from
species.
As suggested by Reznick (2010), a major goal of The
Origin was to present the theory of evolution by natural
selection as an alternative to the prevailing view of species
as the products of special creation. Hence, Darwin’s view
of varieties and species as being interconnected by many
small differences was perhaps more important than establishing just how species originate or how to distinguish
“species” from everything else.
Most evolutionists now define species as reproductively
isolated groups and regard hybrid sterility as just one of
many possible isolating barriers (Dobzhansky 1937, 1951;
Mayr 1942, 1947; Coyne and Orr 2004). Darwin correctly
did not treat hybrid sterility as the sole criterion for species
status, but he also failed to appreciate the role of other
reproductive isolating barriers (Reznick 2010). For practical reasons, reproductive isolation per se is rarely used
as a criterion for diagnosing species status. More often,
morphological and genetic discontinuities between populations serve as proxies for measures of reproductive isolation. Even staunch defenders of the morphological species concept recognize that differences between
populations can arise only if gene flow is limited by ex-
The study of speciation from an evolutionary perspective
is now based almost entirely on reproductive isolation and
thus differs importantly from Darwin’s approach to the
problem (J. A. Coyne, personal communication). Darwin
attempted to delineate the boundaries between varieties
and species by their morphological divergence. That these
differences were often subtle and the interpretation of the
differences arbitrary was a constant source of frustration
to Darwin. The biological species concept (BSC) proposed
by Ernst Mayr made reproductive isolation the principal
criterion for evaluating the taxonomic and evolutionary
status of different populations. Mayr (1942, p. 120) defined
species as “groups of actually or potentially interbreeding
natural populations, which are reproductive isolated from
other such groups.” The BSC has revolutionized the way
we think of species and speciation. Although the BSC is
limited in its applicability to sexual, primarily outcrossing
taxa, it is clearly superior to the morphological species
concept that Darwin accepted.
The BSC provides a general framework for assessing the
taxonomic and evolutionary status of populations. However, until recently, there were no specific guidelines for
how the BSC could or should be implemented to study
the factors contributing to the origin of species. Here I
consider three critical questions in the study of speciation
that are motivated, in large part, by the BSC and review
a method proposed by Coyne and Orr (1989) that holds
great promise for answering them.
First, do populations constitute different species under
the BSC? A standard approach for evaluating species status
is to experimentally cross different populations: if such
crosses fail to yield viable and fertile hybrids, the populations are clearly different species under the BSC. Yet, as
Darwin noted (see above), this criterion is not always sufficient, as some “good” species are capable of producing
fertile hybrids. Mayr (1947, p. 278), concluded, “Most
isolating mechanisms between closely related species that
have been studied thoroughly were found to be multiple.
There always seem to be involved (a) differences in the
ecological requirements, (b) reduction of the mutual sexual stimulation, and (c) reduction in the number and the
Understanding Speciation after Darwin
Adaptation and The Origin
viability of the offspring.” Thus, when any single barrier
is insufficient to prevent gene flow, we need a method that
can quantify the total isolation that is currently, or potentially, achieved through the action of all possible barriers.
Second, what is the contribution of each of the possible
isolating barriers to the current total isolation? For the
most part, studies of speciation have investigated putative
isolating barriers without regard to their actual contribution to the total isolation. One common practice is that
isolating barriers that can function only in sympatry, for
example, mate choice, gametic isolation, and postzygotic
isolation, are commonly measured without consideration
of the geographic distributions of species. Consider a recent study of intrinsic postzygotic isolation between two
allopatric subspecies of fruit flies, Drosophila pseudoobscura
pseudoobscura and D. pseudoobscura bogotana. Phadnis and
Orr (2009) found that a single segregation distorter gene
causes hybrid sterility between these taxa, and concluded
that this is “a strong reproductive barrier between these
young taxa” (p. 376). While this is true, given that these
taxa are allopatric, it seems improbable that hybrid sterility
is a significant barrier to contemporary gene flow, although
it may have contributed to their initial divergence (see
below). Such intrinsic genetic incompatibilities between
allopatric taxa might best be regarded as potential isolating
barriers that could become realized if the two taxa become
wholly or partly sympatric because of changes in their
geographic ranges. Without a method for estimating the
contributions of different isolating barriers to the total
isolation, we risk ascribing speciation to isolating barriers
that may have little or no actual contribution to current
or past isolation.
Finally, which barriers were in place at the time of speciation, that is, when gene flow between taxa essentially
ceases? This is one of the most pressing problems in the
study of speciation. It is one thing to find that a given
barrier explains most of the current isolation between biological species or that it might prevent gene flow if allopatric populations were forced into sympatry, but this
is no assurance that it had the same importance at the
time of speciation.
Answers to these and other questions about the origin
of species can be obtained via the components-of-isolation
method (CIM) developed by Coyne and Orr (1989) and
implemented in their landmark papers on speciation in
Drosophila (Coyne and Orr 1989, 1997). The CIM estimates the contributions of different individual isolating
barriers to the total reproductive isolation between populations or species. The conceptual advance of the CIM
is the recognition that the barriers isolating species or
S11
populations act sequentially throughout the life cycle.1 One
can think of different potential isolating barriers as filters
that act at different life-history stages to reduce gene flow.
Later-acting barriers can eliminate only genes that were
not removed by the action of earlier barriers. Hence, the
contributions of later-acting barriers are “discounted” by
those that precede them.
Coyne and Orr (1989) developed the CIM to compare
the contributions of premating, sexual isolation (Pre), and
intrinsic postzygotic isolation (Post) to the total isolation
between species pairs of Drosophila. Assuming that the two
barriers act sequentially, Coyne and Orr estimated the total
isolation between species (T) as
T p Pre ⫹ (1 ⫺ Pre) Post.
(1)
Ramsey et al. (2003) showed that this approach could be
generalized to multiple barriers. The absolute contribution
(ACn) of a component of reproductive isolation (RI) at
stage n in the life history is
( 冘 )
n⫺1
ACn p RIn 1 ⫺
ACi ,
(2)
ip1
and for m barriers the total isolation is
冘
m
Tp
ACi .
(3)
i⫺1
The CIM provides empirical estimates of (1) the individual
barrier strength, (2) the absolute contribution of each barrier to the total isolation, and (3) the total isolation. To
illustrate, consider how the CIM might be used to assess
the degree of reproductive isolation between two populations and to estimate the current importance of the various isolating barriers. We assume that estimates of the
strength of individual barriers are obtained for habitat
isolation, premating isolation, postmating isolation, and
postzygotic isolation. For simplicity, we also assume that
barrier strength is symmetrical between the taxa and that
barriers evolve at the same rate, such that each barrier has
the same individual strength, with a hypothetical value of
0.80. Thus, in this example, 80% of the potential gene flow
between populations is eliminated by each barrier (fig. 2A).
No single barrier is sufficiently strong to isolate the populations to a level that would satisfy the BSC, yet when
the four barriers are considered together, the total isolation
is very strong (T p 0.998; fig. 2B).
The CIM thus gives an answer to the first question
1
When I asked Coyne about the source of this method, he remarked, “It
was my idea, … but it’s obvious, isn’t it?”
S12 The American Naturalist
Figure 2: Hypothetical example applying Coyne and Orr’s (1989) components-of-isolation method, with modifications from Ramsey et al.
(2003), for estimating the contribution of sequential reproductive barriers
to the total reproductive isolation. A, Individual barrier strengths are the
same (0.80) for each barrier. B, Absolute contribution of each barrier to
the total isolation. Total isolation is the sum of the absolute contributions
for all barriers. See text (eqq. [2], [3]) for methods.
above: Do populations meet the criteria for species status
under the BSC? This could prove particularly useful in
comparisons of allopatric populations where potential isolating barriers are not “tested” in sympatry. Furthermore,
the CIM answers the second question above: What is the
contribution of each of the possible isolating barriers to
the current total isolation? As illustrated in the example
(fig. 2B), we find that habitat isolation, the earliest-acting
barrier, is responsible for most of the total isolation and
that subsequent barriers have progressively lesser roles.
This is despite the fact that each barrier has evolved at the
same rate and has the same individual strength. Finally,
when combined with estimates of time since divergence,
the CIM has the potential to answer the last question
above: Which barriers were in place at the time of speciation? This is an issue with all categories of barriers.
Consider, for example, the challenge in trying to assess the
historical importance of intrinsic postzygotic barriers in
cases where these barriers are currently strong. Were such
barriers also strong at the time of speciation? An example
where this is probably the case is polyploid speciation,
because intrinsic postzygotic isolation is often nearly complete at the time of polyploid formation. Yet new polyploids also display substantial ecological differentiation
from their ancestors (Ramsey and Schemske 2002). Thus,
even in polyploid speciation, intrinsic postzygotic isolation
may not be the primary isolating barrier (Sobel et al. 2010;
see below).
By estimating the contributions of those barriers that
allow nascent populations to achieve complete reproductive isolation, the CIM may offer a way to answer Darwin’s
(1859, p. 111) main question, “How, then, does the lesser
difference between varieties become augmented into the
greater difference between species?” Although I suggest
that the CIM of Coyne and Orr (1989) provides a valuable
framework for evaluating current and historical barriers
to gene exchange, there are some unresolved issues concerning its implementation. For example, Martin and Willis (2007) and Lowry et al. (2008b) suggest that one cannot
treat different barriers as evolutionarily independent and
that reciprocal differences, that is, asymmetries between
the parental taxa in the magnitude of gene flow, must be
considered when estimating the overall effects of different
barriers. On the basis of these and other concerns, Martin
and Willis (2007, p. 78) concluded that “quantitative measures of either total isolation or the proportional contributions of its components appear to be unattainable.”
However, they present no alternative, and for reasons outlined above, I suggest that the CIM is currently the best
approach to evaluate the importance of multiple barriers
to the total isolation between populations and species.
Nevertheless, it is critical that future studies investigate
how the CIM and other methods can be developed for
making these estimates (see below).
Reproductive Isolation in Nature
What is the total reproductive isolation between species
in nature, and what are the primary isolating barriers? To
address this question, I review here empirical studies that
have investigated multiple barriers, largely through implementation of the CIM, to estimate the current total
isolation and its components. This is one approach to
evaluating Darwin’s view that adaptive divergence caused
by natural selection is a major factor in the origin of species. However, it is important to note that the studies
reviewed here examined current barriers and thus do not
necessarily reflect the importance of those barriers that
were in place at the time of speciation. Specifically, I compare the importance of early barriers, such as habitat and
premating isolation, to that of late-acting barriers, such as
postmating prezygotic isolation and postzygotic isolation.
Adaptation and The Origin
S13
This is admittedly an imperfect test of Darwin’s principle
of divergence, as it is well understood that ecological adaptation can contribute to the evolution of late-acting barriers, such as intrinsic postzygotic isolation (see below).
Nevertheless, a finding that ecological barriers can serve
as a major isolating barrier would support the idea that
adaptive divergence is a critical factor in the origin of
species, as Darwin suggested.
A Case Study: Adaptation and Speciation in Mimulus
To illustrate how the CIM can be implemented, I begin
with a description of the relationship between adaptation
and speciation in two closely related species of monkeyflowers, Mimulus lewisii and Mimulus cardinalis (section
Erythranthe, Phrymaceae). These species were first studied
by Hiesey et al. (1971) and have been the subject of numerous field and laboratory experiments designed to investigate the ecological genetics of adaptation and speciation (Bradshaw et al. 1995, 1998; Schemske and Bradshaw
1999; Ramsey et al. 2003; Bradshaw and Schemske 2003;
Angert and Schemske 2005; Angert 2006; Angert et al.
2008).
The bee-pollinated M. lewisii has pale pink flowers with
contrasting yellow nectar guides and a wide corolla with
inserted anthers and stigma (fig. 3A). Mimulus cardinalis
is hummingbird pollinated and has red flowers, a narrow
tubular corolla, reflexed petals, and exserted anthers and
stigma (fig. 3B). In the Sierra Nevada of California, M.
lewisii is found primarily at high elevations and M. cardinalis at low elevations; the two species are sympatric in
a narrow band at midelevations (fig. 3C; Hiesey et al.
1971). Reciprocal-transplant experiments conducted at
sites that span the geographic ranges of the two species in
the Sierra Nevada (fig. 3C) demonstrate strong local adaptation (fig. 3D; Angert and Schemske 2005) because of
physiological differences between the species in their temperature tolerances and flowering phenologies (Angert
2006; Angert et al. 2008). Hence, the fact that the geographic ranges of these species are largely nonoverlapping
is due to adaptive differentiation and represents “ecogeographic isolation” (Schemske 2000; Ramsey et al. 2003;
Sobel 2010), that is, the reduction in gene flow between
populations or species that is due to heritable differences
in their geographic distributions.
F2 hybrids produced by intercrossing M. lewisii and M.
cardinalis were used in field and laboratory studies to examine the floral traits that influence pollinator visitation
and the genetic basis of these traits. Experiments with these
hybrids conducted near the zone of sympatry showed that
the absolute and relative visitation rates by bees are much
lower in plants with high petal carotenoid concentration
(Schemske and Bradshaw 1999). Genetic mapping studies
Figure 3: Studies of adaptation and speciation in two closely related
monkeyflowers, the bee-pollinated Mimulus lewisii (A) and the hummingbird-pollinated Mimulus cardinalis (B; photos: D. W. Schemske, H.
D. Bradshaw). C, Elevational distribution of the species in the Sierra
Nevada Mountains in California (modified from Angert and Schemske
2005). Mimulus lewisii is found from mid-elevations to the timberline,
and M. cardinalis is found from low to mid-elevations: the two species
are sympatric in a narrow band at mid-elevations (gray bar). Boxes indicate the locations of experimental gardens used in reciprocal transplant
studies: Jamestown (JA), Mather (MA), White Wolf (WW), and Timberline (TI). D, Results of reciprocal transplant experiments (modified
from Angert and Schemske 2005). E, Wild-type (WT) flower of M. lewisii.
F, Flower of the M. lewisii near-isogenic line (NIL) in which the genomic
region containing the M. cardinalis allele for petal carotenoid concentration was introgressed into M. lewisii. (E and F reprinted from Bradshaw
and Schemske 2003.)
S14 The American Naturalist
of the F2’s determined that this trait is controlled largely
by a single quantitative trait locus (QTL; Bradshaw et al.
1998). To examine further the genetic control of pollinator
specificity, near-isogenic lines (NILs) were produced in
which the QTL containing the M. cardinalis allele for petal
carotenoid concentration was introgressed into M. lewisii,
and vice versa (Bradshaw and Schemske 2003). The NILs
are thus a reasonable approximation of a single flower
color mutation at the petal carotenoid QTL. Field experiments with the NILs showed that the petal carotenoid
substitution had major effects on pollinator visitation
(Bradshaw and Schemske 2003). In comparison to the M.
lewisii wild type (fig. 3E), the M. lewisii NIL (fig. 3F) had
much lower bee visitation and increased hummingbird
visitation, while the M. cardinalis NIL had much lower
bee visitation than the wild type. Phylogenetic studies and
the predominance of bee pollination in the genus suggest
that hummingbird pollination is the derived condition in
M. cardinalis (Beardsley et al. 2003). Thus, the finding that
the M. lewisii NIL has both lower bee visitation and higher
hummingbird visitation than the wild type suggests that
the single adaptive QTL for petal carotenoid concentration
played a major role in the transition from bee to hummingbird pollination (Bradshaw and Schemske 2003).
Given these findings of adaptive divergence in preferred
habitat and pollinators, it is of interest to determine how
these factors contribute to speciation. Are these and other
ecological factors sufficient to prevent gene flow? A comprehensive study of multiple isolating barriers in this system using CIM found that ecogeographic, pollinator, gametic, and intrinsic postzygotic barriers were individually
strong (Ramsey et al. 2003) but that ecogeographic and
pollinator isolation, in that order, made by far the largest
contributions to the total isolation. These data were reanalyzed here, with revisions made to three barriers, as
outlined in table A1 in the online edition of the American
Naturalist. First, new results from ecological niche modeling caused a revision of the estimate of ecogeographic
isolation upward from 0.587, reported by Ramsey et al.
(2003) and acknowledged there to be an underestimate,
to 0.97 (Sobel 2010). Second, by including an estimate of
expected values, the barrier strength for pollinator isolation was revised from 0.976 to 0.952. Finally, the negative
estimates for F1 biomass reported by Ramsey et al. (2003)
were revised with a newly proposed method where barrier
strengths are bounded between ⫺1 and ⫹1, following Sobel (2010). Although these revisions do alter somewhat
the quantitative estimates, the general conclusions from
Ramsey et al. (2003) are unchanged.
Of the eight barriers investigated, three prezygotic barriers (ecogeographic, pollinator, and gametic) and two
postzygotic barriers (hybrid pollen fertility and hybrid seed
mass) were much stronger than the others (fig. 4A). The
total isolation was estimated as 0.9999 (as compared to
0.9995 in Ramsey et al. 2003), meeting the criterion of the
BSC that these taxa constitute reproductively isolated
groups. Applying the CIM for estimating the components
of isolation illustrates the overriding importance of barriers that act early in the life history. Ecogeographic and
pollinator isolation combined cause strong isolation
(10.99), while the contribution from all other barriers
combined is !0.01 (fig. 4B). Thus, despite substantial reductions in the pollen and seed fertility of F1 hybrids (fig.
4A), these postzygotic barriers contribute little to the total
isolation (fig. 4B) because earlier barriers block most of
the potential gene flow before hybrids are produced.
The ease of crossing the two species in the lab and the
high fertility of F1 hybrids led early workers to question
whether these taxa were valid species under the BSC. Hiesey et al. (1971, p. 24) stated, “From a biosystematic point
of view we are inclined to regard the Erythranthe section
as being composed of only two biologically distinct species,” of which M. lewisii and M. cardinalis were viewed
as conspecifics. Yet these same authors clearly understood
that M. lewisii and M. cardinalis were almost completely
reproductively isolated in nature: “It is evident that the
combined effect of ecological isolation and different pollinating agents serves as an extremely effective barrier to
natural intercrossing between these morphologically very
distinct but genetically highly interfertile species” (Hiesey
et al. 1971, p. 23). As Darwin recognized (see above), the
observation that two populations can form hybrids in experimental crosses is not proof that they should be considered the same species. The Mimulus study is an obvious
case in point. Interspecific hybrids are easily produced in
the lab but are rarely observed in nature (Ramsey et al.
2003). The two species are almost completely reproductively isolated, largely by strong ecological barriers, and,
as final proof of their status as biological species, maintain
their distinct characteristics in sympatry.
Comparative Studies
The results obtained for M. lewisii and M. cardinalis illustrate that ecological differences between these two species are currently the major isolating barriers, consistent
with Darwin’s principle of divergence. To determine
whether this is a general pattern, I reviewed studies in
plants and animals that had estimated multiple barriers.
The findings presented here reveal a general pattern of
strong contributions from early barriers, such as habitat
and premating isolation, and weak evidence for a major
role of postzygotic factors, but further research using a
variety of different approaches is needed to evaluate the
generality of these conclusions.
Adaptation and The Origin
S15
Figure 4: Estimates of the individual strength of eight isolating barriers (A) and their contribution to the total isolation (B) between Mimulus lewisii
and Mimulus cardinalis, from the components-of-isolation method (CIM) of Coyne and Orr (1989) as modified by Ramsey et al. (2003). Data are
from Ramsey et al. (2003), with revisions of the individual barrier strengths for ecogeographic isolation, pollinator isolation, and F1 biomass (see
text and table A1 in the online edition of the American Naturalist). Values presented are the means of the estimates of individual barrier strength
for each species (A) and the mean contribution to the total isolation (B). See text and table A1 for details of the calculations and the data. Barriers
are defined as follows: (1) ecogeographic isolation, heritable differences in the geographic range of populations or species due to local adaptation;
(2) pollinator isolation, the reduction in interspecific gene flow in sympatry due to pollinator specificity; (3) gametic isolation, the reduction in F1
hybrid formation due to gametic competition and/or the failure of hybrid zygotes to form mature seed; (4) germination, the percentage difference
in seed germination between F1 hybrids and their parents; (5) flowering, the percentage difference in survival to flowering between F1 hybrids and
their parents; (6) biomass, the percentage difference in biomass between F1 hybrids and their parents; (7) pollen, the percentage difference in the
pollen viability between F1 hybrids and their parents; and (8) seed mass, the percentage difference in the seed mass between F1 hybrids and their
parents.
Plants. Drawing on the review of Lowry et al. (2008b) and
subsequent studies, I compiled data on barrier strength in
plants for studies that examined multiple intrinsic isolating
barriers and estimated the strength of at least one barrier
in each of four different categories: (1) habitat isolation,
(2) premating isolation, (3) postmating isolation, and (4)
postzygotic isolation. Habitat isolation is defined here as
the reduction in gene flow caused by differential adaptation to habitat, either on the scale of the geographic range
(ecogeographic isolation) or at the scale of local populations (microhabitat). Premating isolation is the reduction
in gene flow in sympatry due to temporal isolation (differences in flowering time), pollinator isolation, floral mechanical isolation, and/or the mating system. Adopting a
strict definition of postmating isolation is problematic,
because the failure to produce viable seed in interpopulation crosses could be due to gametic competition and/
or the failure of fertilized ovules to develop. The studies
reviewed here differed in how they classify postmating
barriers to F1 hybrid formation. Ramsey et al. (2003) and
Kay (2006) have strong evidence of gametic isolation as a
cause of reduced interspecific seed production and treated
this as a prezygotic barrier, while Lowry et al. (2008b)
considered a reduction in F1 seed production after mating
to be a postzygotic barrier. G. Chen (personal communication) estimated both gametic isolation and intrinsic
isolation as factors in the failure of interspecific seed set.
Here I classify postmating barriers as the reduction in F1
hybrid formation that is due to gametic isolation. Finally,
postzygotic isolation is defined as the reduction in F1 hybrid formation after interpopulation crosses (but see
above) and/or the percentage difference in the relative fitness of F1 hybrids as compared to the parents for extrinsic
(ecological unfitness of F1 hybrids) and/or intrinsic (F1
hybrid genetic incompatibilities) isolation.
Of the six taxon pairs in Lowry et al. (2008b, table 1)
that met this criterion, Iris fulva–Iris brevicaulis and Phlox
cuspidata–Phlox drummondii were excluded from further
analysis. In the former pair, individual barrier strengths
were reciprocally negative for three of the six barriers in-
S16 The American Naturalist
vestigated (immigrant inviability, F1 seed set, and extrinsic
postzygotic isolation; Lowry et al. 2008b). This would
mean that each taxon and the F1 hybrids perform better
in the habitat of the other taxon and that the F1 hybrids
produce more seed than both parents. If these are in fact
different biological species, other important isolating barriers were probably missed. For the Phlox species pair, a
quantitative estimate of premating isolation was available
for only one of the species. Although the study of geographic adaptation in ecotypes of Mimulus guttatus by
Lowry et al. (2008a) lacked an estimate of barrier strength
for postmating isolation, it was included in the analysis
because premating isolation was complete; hence, the contribution of postmating isolation to the total would be 0
regardless of its individual strength. Two additional taxon
pairs not in the review by Lowry et al. (2008b) were included in the analysis; Husband and Sabara’s (2004) study
of reproductive isolation between diploid and tetraploid
populations of Chamerion angustifolium and a study of the
Neotropical gingers Costus villosissimus and Costus allenii
(G. Chen, unpublished data).
In total, seven taxon pairs were used in the comparative
analysis of reproductive isolation presented here. In addition to those discussed above for M. lewisii and M. cardinalis, several corrections and improvements to the original data were made before calculating the parameters
presented here (table A1). The studies differed in the number of individual barriers investigated, so for purposes of
comparison, I first calculated the strength of isolation for
each of the four barrier categories discussed above, that
is, habitat, premating, postmating, and postzygotic isolation. This was accomplished by applying the CIM approach to each category (Lowry et al. 2008b; G. Chen,
personal communication). I then estimated the total isolation and the contribution to the total isolation (eq. [3]).
Table A1 gives the individual strengths and contributions
to the total isolation for all measured barriers, and table
A2 gives the comparable results for the four barrier
categories.
Although there is considerable scatter, the individual
strength of early-acting barriers such as habitat and premating isolation is typically greater than that for postzygotic isolation (fig. 5A). For all taxa considered together,
the mean barrier strength was highest for habitat isolation
(0.7482) and premating isolation (0.7840), followed by
postmating (0.5685) and postzygotic isolation (0.3914).
The mean total isolation estimated by the CIM for the
seven pairs of plant taxa is 0.9899 (range 0.9591–1.00),
indicating strong barriers to gene flow. In those cases
where the estimated total isolation is incomplete (i.e.,
!1.00), it seems highly probable that one or more isolating
barriers were missed. That partially sympatric taxa such
as Costus pulverulentus and Costus scaber (Kay 2006) and
Figure 5: Summary of individual isolating barriers and the components
of the total isolation for plant studies that estimated multiple isolating
barriers. Numbers refer to the taxa studied; T p total isolation. 1, Mimulus lewisii–Mimulus cardinalis: T p 0.9999. 2, Costus pulverulentus–
Costus scaber: T p 0.9970. 3, Costus allenii–Costus villosissimus: T p
0.9917. 4, Chamerion angustifolium, diploids and tetraploids: T p
0.9950; 5, Ipomopsis aggregata–Ipomopsis tenuituba: T p 0.9871; 6, Iris
fulva–Iris hexagona: T p 0.9591 ; 7, Mimulus guttatus, coastal and inland:
T p 1.00. A, Mean barrier strength for four composite barriers. The filled
symbols represent the grand mean across all seven taxa. B, Contribution
to the total isolation. The filled symbols represent the grand mean across
all seven taxa. See text and tables A1, A2 in the online edition of the
American Naturalist for details.
Adaptation and The Origin
diploid and tetraploid C. angustifolium (Husband and Sabara 2004) retain their genetic and morphological discontinuities despite an estimated total isolation that is !1.00
strongly implicates unmeasured barriers. For example, neither of these studies estimated extrinsic postzygotic isolation. However, even where all possible barriers are examined, the total isolation estimated may be inadequate
to maintain independent gene pools, that is, if Nem 1 1.
In this regard, estimates of historical patterns of gene flow
using molecular genetic markers (Wakeley and Hey 1997;
Counterman and Noor 2006; Strasburg and Rieseberg
2008) would be useful for evaluating the population genetic consequences of different levels of total isolation as
estimated by the CIM (see below).
On average, the contribution to the total isolation drops
substantially with each successive stage of isolation (fig.
5B). For all taxa considered together, the mean contributions are 0.7482, 0.2056, 0.0309, and 0.0053 for habitat,
premating, postmating, and postzygotic isolation, respectively. A decline in the contribution to the total isolation
from early to late in the life history is expected because
late-acting barriers can prevent only the gene flow remaining after the action of earlier barriers (fig. 2). However, the greater strength of earlier barriers for the plant
studies reviewed here (fig. 5A) also contributes to the observed decline in barrier strength.
For six of the seven studies included here, the contribution from habitat isolation was higher than that of any
other stage. The one exception is the I. fulva–Iris hexagona
species pair, for which there is no estimate of ecogeographic or microhabitat isolation using spatial distribution
data, although a reciprocal-transplant study showed only
weak habitat isolation (immigrant inviability in table 1 of
Lowry et al. 2008b). That habitat isolation has by far the
strongest contribution to the total isolation is consistent
with Darwin’s focus on adaptation to different habitats as
a major cause of speciation, yet it must be emphasized
again that current barrier strengths may differ from those
at the time of speciation.
Six of the seven studies obtained estimates of intrinsic
postzygotic isolation, but in only two cases is this barrier
strong (table A1). The two exceptions are the M. lewisii–
M. cardinalis species pair, where the strength of postzygotic
isolation is strong (10.50) for F1 pollen viability and F1
seed mass (fig. 4A), and diploid and tetraploid C. angustifolium, where intrinsic postzygotic isolation is 0.87,
stronger than all other measured barriers (table A1). Nevertheless, even in these two systems the contribution of
intrinsic postzygotic isolation to the total isolation is low
(!0.1; tables A1, A2) because strong habitat and pollinator
isolation stop virtually all gene flow before F1 hybrid
formation.
As exemplified by Husband and Sabara’s (2004) study
S17
of diploid and tetraploid C. angustifolium, crosses between
ploidy levels typically produce sterile hybrids. This potential isolating barrier evolves immediately with polyploidization (Ramsey and Schemske 1998, 2002). These observations led Schluter (2001) to suggest that polyploid
speciation is nonecological. However, strong postzygotic
isolation may actually hinder polyploid establishment.
Consider that the first polyploids are almost certainly rare.
Thus, in the case of sexual and outcrossing taxa, new polyploids will mate primarily with their ancestors and produce
largely sterile offspring. All else being equal, this negative
frequency dependence, that is, minority-cytotype exclusion (Levin 1975), will cause the rapid extinction of new
polyploids unless there are other isolating barriers in place.
Spontaneous polyploids often differ substantially from
their ancestors in a number of ecological and physiological
traits (Ramsey and Schemske 2002) that may cause immediate habitat isolation. In this regard, it is interesting
that Husband and Sabara (2004) found that habitat isolation had the strongest contribution to the total isolation
between diploid and tetraploid populations of C. angustifolium. When considered individually, intrinsic postzygotic isolation was strong, yet this barrier had only a small
contribution to the current total isolation (fig. 5; table
A1). Regrettably, despite its importance, polyploid speciation is almost entirely unexplored and deserves further
attention.
The C. villosissimus–C. allenii species pair is a striking
example of Darwin’s proposal for the origin of plant species by adaptation to different soil moisture environments
(Darwin’s diagram depicted in fig. 1). These two species
of Neotropical gingers are each other’s closest relatives
(Kay et al. 2005), use the same pollinators (euglossine
bees), and are often found within close proximity but occupy very different habitats. Costus allenii inhabits dense
forest understory along streams, while C. villosissimus is
found in drier sites with less canopy cover (G. Chen, personal communication). That these differences reflect local
adaptation was confirmed by extensive reciprocal-transplant experiments (G. Chen, unpublished data). The two
species are easily crossed to produce fully fertile F1 hybrids,
yet their strong local habitat differentiation (microhabitat
isolation 1 0.90; table A1) results in a microallopatric distribution that greatly reduces gene flow. Laboratory and
field experiments show that differences in drought tolerance and the timing of seed germination contribute to
their spatial isolation (G. Chen, personal communication)
and indicate that local adaptation to edaphic factors has
played an important role in adaptation and speciation in
these taxa.
As further evidence of the importance of adaptive habitat differentiation in the origin of plant species, Sobel
(2010) employed ecological-niche modeling (see Sobel et
S18 The American Naturalist
al. 2010) to examine the role of environmental factors such
as temperature, precipitation, and geology to the spatial
distributions of 12 pairs of phylogenetically independent
sister species in the genus Mimulus. He found strong or
complete ecogeographic isolation in seven of the species
pairs and moderate ecogeographic isolation in five pairs.
The average individual strength of ecogeographic barriers
was 0.641. By contrast, the mean barrier strength for pollen
viability of F1 hybrids, a common measure of intrinsic
postzygotic in plants, was just 0.004 (Sobel 2010). These
data strongly suggest that habitat isolation has been more
important than intrinsic postzygotic isolation in the speciation of these young taxa.
In their review of 19 plant systems, some of which are
included here, Lowry et al. (2008b) found that the absolute
strength of prezygotic barriers was, on average, twice that
of postzygotic barriers, and in reviewing the components
of isolation in several different plant systems, Rieseberg
and Willis (2007) also concluded that early-acting barriers
are the most important. The total isolation and its components were not estimated in either of these studies. Nevertheless, their findings, and the analysis presented here,
strongly suggest that early-acting barriers such as habitat
and premating isolation are the principle isolating barriers
in plants.
Animals. At present, few studies in animals have estimated
multiple components of reproductive isolation. The original papers on Drosophila by Coyne and Orr (1989, 1997)
examined one prezygotic barrier, mating discrimination,
and two postzygotic factors, the viability and fertility of
male and female F1 hybrids, all measured under laboratory
conditions. They concluded that both prezygotic and postzygotic isolation increase with genetic distance between
species pairs, a surrogate for time, and that prezygotic
isolation evolves more quickly in sympatric than in allopatric taxa, a conclusion consistent with selection for reinforcement in sympatry. Of the species pairs investigated
in their studies, 150% are allopatric (from table 1 in Coyne
and Orr 1989 and table 1 in Coyne and Orr 1997), yet
the barriers they examined can come into play only in
sympatry. Hence, the studied barriers do not currently
contribute to reproductive isolation in allopatric species,
although they may become important if these taxa became
sympatric. Their finding that there is little or no intrinsic
postzygotic isolation for many “young” species pairs with
low genetic divergence (fig. 1b in Coyne and Orr 1997)
may suggest that this putative barrier evolves mainly after
speciation is complete (Mallet 2006). A similar pattern is
seen in Lepidoptera, in which intrinsic postzygotic isolation accumulates with time, yet the youngest species display little or no postzygotic isolation (fig. 1 in Presgraves
2002).
Other studies of isolating barriers in animals also suggest
that intrinsic postzygotic isolation may play little role in
the origin of species. For example, in their review of intrinsic postzygotic isolation in birds, Price and Bouvier
(2002, p. 2088) concluded that “genetic incompatibilities
causing F1 infertility and F1 inviability in captivity often,
but not always, arise after the speciation process is essentially complete.” In a study of freshwater fish (Percidae:
Etheostoma), Mendelson (2003, p. 317) concluded that sexual isolation due to strong sexual selection “will tend to
evolve to completion before hybrid inviability, strictly as
a by-product of divergence in geographically isolated populations.” Similarly, Bolnick and Near (2005) found that
intrinsic hybrid inviability in centrarchid fish, measured
under laboratory conditions, does not appear until approximately six million years after divergence, and they
concluded that “the evolution of hybrid inviability plays
little role in driving speciation in centrachids” (p. 1765).
Two recent studies investigating multiple potential barriers in animals also find a greater importance of earlyacting barriers. Matsubayashi and Katakura (2009) investigated premating, postmating, and postzygotic barriers
between two closely related ladybird beetles (Henosepilachna spp.) and found that reproductive isolation is nearly
complete, largely because of habitat isolation. Similarly,
Dopman et al. (2009) investigated multiple potential isolating barriers between strains of the North American corn
borer (Ostrinia nubilalis) and found that much of the total
isolation is caused by premating barriers, particularly temporal and behavioral isolation.
Summary: Reproductive Isolation in Nature
The pattern that emerges from this admittedly incomplete
review is that the most closely related populations and
species are isolated primarily by ecological barriers that
prevent hybrid formation. While the individual strength
of intrinsic postzygotic factors is sometimes large, the current contribution of these late-acting barriers to the total
isolation is usually very small. These findings are consistent
with Darwin’s principle of divergence, that the origin of
species is achieved largely through ecological adaptations.
Obviously, more studies are needed to determine whether
these are general patterns and whether current barriers
were important at the time of speciation.
Future Directions
Some 150 years after publication of The Origin, substantial
controversy remains over the nature of speciation. With
the extraordinary achievements made since Darwin in
fields such as genetics, ecology, population biology, and
systematics, there is now an unprecedented opportunity
Adaptation and The Origin
to answer many of the most pressing and difficult questions concerning the origin of species. Here I discuss some
fertile areas for further research.
What Are the Traits That Contribute to
Reproductive Isolation, and What Is
the Genetic Basis of These Traits?
Darwin emphasized the relationship between adaptive divergence and the origin of species, but as discussed above,
he did not link adaptation to reproductive isolation. As a
result, in large part, of the new focus on ecological speciation (Schluter 2001, 2009; Rundle and Nosil 2005), we
now have a number of examples of how the traits involved
in adaptive divergence contribute directly to reproductive
isolation (Schemske and Bradshaw 1999; Rundle et al.
2000; Nosil 2007). However, we do not know how often
the traits that are the direct targets of natural selection
might also contribute to the evolution of reproductive
barriers that are manifest at other stages in the life history.
These indirect effects (Coyne and Orr 2004) or by-products (Sobel et al. 2010) of adaptive divergence could play
an important role in speciation (Coyne and Orr 2004;
Nosil et al. 2009; Sobel et al. 2010). For example, the genes
involved in adaptation to copper-rich soils on mine tailings
may also play a role in hybrid incompatibilities between
Mimulus populations growing on and off copper mines
(Christie and Macnair 1987). And in Drosophila, there is
evidence that the lethality of hybrids between Drosophila
melanogaster and Drosophila simulans is due to adaptive
divergence in their nuclear-pore proteins (Presgraves et al.
2003). Thus, adaptive substitutions may contribute to several potential isolating barriers, including hybrid incompatibilities.
Linking adaptive traits to reproductive isolation is just
one step toward identifying the origin of species. The next
is to investigate the genetic basis of those traits. How many
genetic changes are required for speciation? How do the
genes that cause reproductive isolation evolve? Do isolating
barriers differ in their genetic makeup? How much reproductive isolation is achieved though the substitution
of individual “speciation genes”? The remarkable discoveries in genetics since Darwin now make it possible to
identify genes and genomic regions that contribute to speciation (Noor and Feder 2006; Lexer and Widmer 2008).
Examples include studies of floral traits and pollinator
isolation in Mimulus (Bradshaw et al. 1998; Bradshaw and
Schemske (2003) and Iris (Bouck et al. 2007) and of hybrid
incompatibilities in Iris (Taylor et al. 2009), Mimulus
(Fishman and Willis 2006), Helianthus (Rieseberg et al.
1999), and Drosophila (Presgraves et al. 2003; Orr et al.
2004; Presgraves 2010a, in this issue). One promising approach that deserves further attention is the use of near-
S19
isogenic lines (NILs) to study the relationship between
traits, genes, and reproductive isolation. NILs are created
by moving small genomic regions containing an allele from
one species into the genome of another. The NILs and
their associated wild-type lines can be employed in field
or laboratory experiments to estimate the change in phenotype and the strength of isolation that might be experienced after a single substitution.
For example, NILs created for petal carotenoid concentration in Mimulus (fig. 3E, 3F) revealed that substantial
pollinator isolation is achieved after the substitution of
what is essentially a single gene (Bradshaw and Schemske
2003). Ortı́z-Barrientos and Noor (2005) used a similar
approach to verify that a single genomic region has a large
effect on premating isolation in Drosophila pseudoobscura
and Drosophila persimilis. Further studies using these approaches could determine the direct and indirect effects
of adaptive substitutions on reproductive isolation (Nosil
et al. 2009; Sobel et al. 2010) and ultimately estimate the
number of genes required for speciation.
What Is the “Importance” of Different Isolating Barriers
at the Time of Speciation?
Reproductive isolating barriers continue to evolve once
speciation is complete; thus, studies of current barriers
may not reflect those in place at the time of speciation.
Identifying the barriers that contributed to speciation is
particularly challenging if one or more barriers are currently strong enough to cause complete isolation: Were
they also in place at the time of speciation, or did they
evolve after speciation was complete?
To answer this question will require studies that examine
the full range of potential isolating barriers in nascent and
recently diverged species. One possible approach is to identify pairs of sister taxa, from nascent to young species, and
to then estimate the contributions of all isolating barriers
to the total isolation for each pair. A regression of the
contribution to the total isolation against time since divergence for each barrier gives an estimate of its rate of
evolution. The importance of the different barriers present
at the time of speciation could then be estimated at the
point where the total isolation summed across all barriers
approaches 1.00. Such studies are difficult to implement
because of the many different pieces of information required, from phylogenetic studies of species relationships
to field and lab studies estimating barrier strengths and
the contributions of individual barriers to the total isolation.
S20 The American Naturalist
What Is the Role of Ecogeographic Isolation in Speciation?
Although microhabitat isolation is widely acknowledged
as an important isolating barrier (Coyne and Orr 2004),
ecogeographic isolation, defined here as heritable differences in the geographic range of populations or species
due to local adaptation, is not. This reflects a contradiction
in our current approach to the study of speciation. On
the one hand, most researchers acknowledge that allopatric
speciation, that is, the evolution of essentially complete
reproductive isolation after the geographic isolation of
populations by extrinsic barriers (e.g., mountains, rivers,
climate change), is probably the major mechanism of speciation (Coyne and Orr 2004). Yet during the period of
geographic isolation, we may often expect the evolution
of intrinsic ecological barriers that might maintain allopatry even if the original extrinsic barriers were to disappear. This ecogeographic isolation has long been recognized as a legitimate isolating barrier (Coyne and Orr
2004; Sobel et al. 2010), but until very recently it has not
been included in empirical studies of speciation. If most
speciation begins (and often ends) with complete geographic isolation, why would we not estimate ecogeographic isolation in allopatric species?
One obvious answer is that it may be difficult to distinguish historical from biological causes of allopatry. The
important distinction between history and adaptation in
evaluating geographic isolation as a potential barrier was
probably first recognized by Dobzhansky (1937), who
noted that “the occupation of separate areas by two species
may be due not only to the fact that they have developed
there, but also to the presence of physiological characteristics that make each species attached to the environment”
(p. 231). Mayr (1947), too, recognized that geographical
and ecological differences often go hand in hand, citing
as an example the “geographical-ecological” races of the
mistle thrush in Europe. Stebbins (1950) applied this same
idea to plant distributions, and Coyne and Orr (2004)
acknowledged that both micro- and macrospatial habitat
isolation can contribute to speciation.
Thus, it is not so much that evolutionists doubt the
importance of ecogeographic isolation; it seems instead
that because of the difficulty in estimating this barrier,
they have simply neglected it. A number of approaches to
the problem have been considered, each with its own set
of advantages and disadvantages. The classic approach of
reciprocal-transplant experiments is definitive but also
raises conservation concerns if habitats are disrupted and/
or nonnative genotypes are introduced. Ecological-niche
modeling is a new approach that has great promise for
asking whether historical factors, ecological adaptations,
or both cause allopatric distributions (Sobel et al. 2010).
This method might prove the only means available to study
species of conservation concern or those where a reciprocal
transplant is impractical. Yet it requires comprehensive
data on species distributions, is difficult to apply to rare
species, and requires that the major determinants of the
geographic distribution have been enumerated at a relatively fine spatial scale. Finally, Nosil et al. (2005) have
recently proposed that “immigrant inviability” be considered as a measure of isolation due to local adaptation.
They define immigrant inviability as “the reduced survival
of immigrants upon reaching foreign habitats that are ecologically divergent from their native habitat” (p. 705). As
discussed by Sobel et al. (2010), the procedure for estimating immigrant inviability seems no different from that
for evaluating local adaption by a reciprocal-transplant
experiment.
One important parameter left out of all of these approaches is the migration rate between populations. By
combining studies of ecogeographic isolation with estimates of migration rates, it should be possible to partition
the total ecogeographic isolation into that due to failure
to migrate and that due to the failure of migrants to establish. Ecogeographic isolation is essentially the product
of these two parameters. This is an important area of future
research.
When Is Speciation Nonecological?
Recently, Schluter and colleagues (Schluter 2001, 2009;
Rundle and Nosil 2005) made the connection between
adaptation and barriers to gene flow that Darwin missed.
They define ecological speciation as “the evolution of reproductive isolation between populations or subsets of a
single population by adaptation to different environments
or ecological niches” (Schluter 2009, p. 737). All other
means of evolution of isolating barriers, for example, uniform natural selection, genetic drift, and polyploidy, are
considered nonecological mechanisms (Schluter 2001).
The ecological-speciation perspective has stimulated a
wave of new research on the role of ecological factors in
speciation. Recent examples include studies of body size
and premating isolation in sticklebacks (McKinnon et al.
2004) and host plant adaptation in walking sticks (Nosil
2007). Moreover, in a review of ecological divergence in
a variety of plants and animals, Funk et al. (2006) concluded that, controlling for time, reproductive isolation is
greater in those groups with the greatest ecological divergence. Yet Hendry (2009) suggests that few studies of ecological speciation have employed adequate methods. And
Sobel et al. (2010) question whether the ecologicalspeciation perspective presents a false dichotomy, suggesting that the putative examples of nonecological speciation (uniform selection, genetic drift, polyploidy) also
involve ecological processes (although these mechanisms
Adaptation and The Origin
are “nonecological” in that they do not require divergent
natural selection).
Nevertheless, nonecological speciation is theoretically
possible. Price (2008) proposed a hypothetical scenario
whereby sexual selection in birds can cause reproductive
isolation between populations without ecological divergence. Evidence for such a mechanism comes from studies
of Enallagma damselflies by McPeek and colleagues. They
find that species are ecologically equivalent (Siepielski et
al. 2010) and that coexistence of multiple species in sympatry is due largely to mate choice and divergence in mating structures (McPeek et al. 2008). Schluter (2009) suggested that even where populations experience the same
selection pressures, the fixation of different adaptive mutations in different populations could lead to speciation,
a mechanism termed “mutation-order” speciation. And
there is also growing evidence that intrinsic postzygotic
reproductive isolation (hybrid sterility and inviability) can
evolve as the incidental by-product of intragenomic conflicts between selfish genetic elements and their host
genomes (Johnson 2010; Presgraves 2010a, 2010b). Intragenomic conflicts, which occur without regard to ecological setting, represent a special case of mutation-order speciation in which selfish genes and host genomes experience
recurrent bouts of coevolution. Studies are needed that
investigate the likelihood of these and other proposed nonecological mechanisms of speciation.
How Do We Best Evaluate the Strength of Isolating
Barriers and Their Importance in Speciation?
Here I have argued that estimating total isolation and the
contribution of different barriers to the total isolation is
critical for understanding the importance of current and
historical isolating barriers. While acknowledging the need
for such an approach, Martin and Willis (2007) identified
several issues that merit further attention, including methods for evaluating asymmetries in barrier strength, comparing observed to expected isolation, and estimating total
isolation if barriers are not independent. Another potential
problem is in evaluating extrinsic and intrinsic postzygotic
isolation: the latter is typically estimated under benign
laboratory conditions, and it is not clear how one might
distinguish it from extrinsic isolation, which is estimated
in nature (T. Price, personal communication).
These concerns highlight the need for investigating alternative approaches for estimating the importance of different isolating barriers. In particular, studies are needed
that adopt a population genetic framework for estimating
barrier strength, such as those proposed by Barton and
Bengtsson (1986) and Gavrilets and Cruzan (1998). In
addition, estimates from alternative methods must be
compared, for example, estimates of total isolation using
S21
the CIM of Coyne and Orr (1989) and gene flow estimates
obtained from coalescent models of genetic data, as proposed by Wakeley and Hey (1997). This would allow the
important test of whether isolation estimates such as those
presented here are predictive of current and/or historical
levels of introgression. In this regard, Sobel (2010) recently
implemented such a study in two species pairs of Mimulus
and, consistent with expectation, found greater introgression between the taxa that had the lowest estimate of total
isolation.
What Is the Fate of Populations or Species That
Experience Reduced Reproductive Isolation Due
to Geologic or Environmental Perturbations?
Under some circumstances, young species may not possess
sufficient irreversible isolation to prevent collapse if extrinsic geographic barriers are erased or environmental
conditions change. One approach to this problem is to
compare the total isolation that would result solely from
the action of irreversible barriers, such as intrinsic genetic
incompatibilities in F1 and later-generation hybrids, to that
realized by all barriers. This would provide a means of
identifying where populations lie along a continuum of
speciation states (Hendry 2009). For example, the collapse
of a sympatric stickleback species pair is thought to be a
result of extensive introgression after a decline in water
clarity attributed to an invasive crayfish (Taylor et al.
2006). In this system, it appears that sexual isolation
achieved through visual mating cues was a reversible premating barrier and that irreversible postzygotic barriers
were insufficient to prevent gene flow after the environmental perturbation. Studies are needed that examine the
fate of taxa after perturbation: will they fuse, or will they
maintain separate gene pools through the evolution of
additional isolating barriers, that is, reinforcement (Noor
1999; Servedio and Noor 2003; Kay and Schemske 2008)?
Moreover, in the case of collapse, should we regard the
taxa as “good” biological species before the perturbation?
Do the Rates and Mechanisms of Speciation Differ
in Different Geographic Regions, and If So, What
Might Be the Consequences for Broad Patterns
of Community Diversity?
Speciation is the source of organismal diversity, and therefore study of the origin of species should figure prominently in discussions of the factors that contribute to geographic patterns in community diversity. For the most
part, this is not the case. An obvious example is the longstanding debate over the cause of the latitudinal diversity
gradient (LDG). Discussions on this topic have focused
almost exclusively on ecological factors that might influ-
S22 The American Naturalist
ence the maintenance of species and far less on species
origins (Mittelbach et al. 2007; Schemske 2009). Recent
hypotheses propose higher speciation rates in equatorial
regions due to higher temperatures (Allen et al. 2006) or
to a greater importance of biotic interactions (Schemske
2009; Schemske et al. 2009), and new phylogenetic approaches hold great promise for assessing geographic patterns in rates of speciation (Weir and Schluter 2007; Ricklefs 2009). Yet there is surprisingly little discussion of how
speciation might contribute to the LDG or to other geographic patterns of diversity.
Darwin, The Origin, and the Next Naturalists
When the views advanced by me in this volume, and by Mr.
Wallace, or when analogous views on the origin of species are
generally admitted, we can dimly foresee that there will be a
considerable revolution in natural history. (Darwin 1876, p.
425)
In the final edition of The Origin, Darwin (1876, p. 424)
speaks to the profound impact of his theory of natural
selection: “I formerly spoke to very many naturalists on
the subject of evolution, and never once met with any
sympathetic agreement. … Now things are wholly
changed, and almost every naturalist admits the great principle of evolution.” Some 150 years later, much remains
to be done. What are the traits that contribute to speciation? What is the genetic basis of these traits? Which
isolating barriers are most “important”?
There are now unparalleled opportunities to combine
ecological, phylogenetic, and molecular genetic approaches
to answer these and other persistent questions. The study
of speciation, as the engine of biodiversity, must be considered one of the fundamental disciplines in biology. Yet
the rapid loss of intact natural habitats and the increased
fragmentation of those that remain make time of the essence if we wish to make further progress in understanding
the mechanisms of speciation. Darwin entrusted young
naturalists to pursue the many questions about the origin
of species that he left unanswered (1876, p. 423): “I look
with confidence to the future,—to young and rising naturalists, who will be able to view both sides of the question
with impartiality.” I too am hopeful that the next generation of naturalists will further our understanding of what
Darwin (1859, p. 1) called “that mystery of mysteries.”
Acknowledgments
I thank G. Chen, J. “King” Coyne, D. Pfennig, D. Presgraves, J. Sobel, L. Watt, and J. Willis for discussion and
G. Chen, J. Coyne, E. Dittmar, C. Johnston, K. Kay, T.
Price, J. Sobel, and an anonymous reviewer for valuable
comments on the manuscript. Funding was provided by
National Science Foundation grant DBI-0328636. This is
contribution number 1567 from the W. K. Kellogg Biological Station.
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