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Reproductive isolation: Natural selection at work
Brian Charlesworth and Deborah Charlesworth
t-
Although much is known about the genetic basis of
reproductive isolation between species, little is understood
about its underlying evolutionary causes. A study of two
very closely related, but reproductively isolated, plant
species has provided some valuable insights.
Address: Institute of Cell, Animal and Population Biology, University
of Edinburgh, Ashworth Laboratories, King’s Buildings, West Mains
Road, Edinburgh EH9 3JT, UK.
Current Biology 2000, 10:R68–R70
0960-9822/00/$ – see front matter
© 2000 Elsevier Science Ltd. All rights reserved.
The crucial step in the separation of two populations of a
sexually reproducing species into two new species —
speciation — is the acquisition of reproductive isolation
between them. Such isolation ensures that they can evolve
independently of each other, and so end up with radically
different genotypes and phenotypes. This causes the
biological world to be divided up into the discrete
taxonomic groups which we take for granted. Many
different ways in which populations can fail to interbreed
have been described, ranging from simple ecological
separation of time or place of breeding, through behavioural barriers to interbreeding, to inviability or infertility
of hybrids [1].
Reproductive isolation has long been thought to evolve
mainly as a by-product of the divergence of populations
that are prevented from interbreeding by external barriers
such as spatial separation. There is clearly no selection to
maintain compatibility of mating behaviour between individuals from geographically or ecologically separated populations, or to maintain harmonious interactions between
genes that have acquired different alleles in different populations. Given enough evolutionary divergence between
populations, complete reproductive isolation may therefore be expected to arise [1]. This is no more surprising in
principle than the fact that electrical plugs of British
design do not function in Continental European sockets.
While this simple model is consistent with most of the
facts relating to the genetics and ecology of reproductive
isolation, it leaves several important questions
unanswered. These include the amount of restriction on
gene flow that will permit enough divergence for
reproductive isolation to evolve, the time-scale needed
for speciation to be completed, the genetic basis of reproductive isolating barriers, and the causes of the evolutionary divergence that drives reproductive isolation. More or
less complete answers to the first three questions are
available. In many ways, the last question is the hardest
to answer, as it is usually impossible to relate a particular
example of reproductive isolation to the underlying evolutionary forces, even if we have considerable knowledge
of its genetic basis.
Pollinator preferences can lead to reproductive isolation
between flowering plant species, and may provide good
examples for studying the evolutionary origin of the features
that lead to new species formation [2,3]. A recent study of a
pair of closely related plants, Mimulus lewisii and M. cardinalis, has examined the adaptive evolution of their reproductive isolation [4]. Most species in the monkeyflower
genus Mimulus are pollinated by bees, and their floral morphology can be interpreted as a set of adaptations to this
mode of pollination, as in the case of M. lewisii (in which
100% of 233 visits observed in a natural population were by
bees) [4]. In some cases, however, there has been a shift to
pollination by hummingbirds, as in M. cardinalis (with more
than 97% of 146 visits from hummingbirds).
The change to pollination by hummingbirds in M.
cardinalis is accompanied by a set of changes in the
flowers (Figure 1, Table 1). These changes have almost
certainly been driven by selection for more effective
attraction of hummingbird pollinators. Similar differences
between species with different pollinators are common in
plant genera [5–7], and hummingbird pollinated species
have repeatedly and independently evolved tubular
flowers, often with orange or red colours different from
those of their congeners [7–9]. In the case of the two
Mimulus species, observations on pollinator behaviour in
the wild suggest that there is little chance that a bee that
Figure 1
Flower morphology of the two Mimulus species studied by Schemske
and Bradshaw [4]. (Images courtesy of Douglas Schemske.)
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Table 1
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Figure 2
Floral characteristics of the two Mimulus species studied.
Species
M. lewisii
M. cardinalis
Pollinators
Bee
Hummingbird
Flower size
Small
Large
Flower shape Wide, with ‘landing platform’
Narrow
Flower colour
Pink (low carotenoids)
Red (high anthocyanins)
Nectar
Moderate, high sugar
Abundant, low sugar
has visited M. lewisii will subsequently visit M. cardinalis,
or that a hummingbird that has visited M. cardinalis will
visit M. lewisii [4].
A cross between the two Mimulus species, made for the
purpose of analysing the genetics of the traits distinguishing them [10], has now provided an unusual opportunity
for testing the relation between phenotype and pollinator
preference, and the effect of this on the degree of reproductive isolation between them [4]. The F2 hybrid plants
show a wide range of flower colours and morphological
differences. To test their effects on pollinators, arrays of
plants were placed in the field at a locality where both
plant species, and both kinds of pollinators, coexist.
Because the species differ at a number of loci controlling
several independent characters, many different character
combinations are produced, so that the effects of individual floral characteristics can be separately analysed, using
multiple regression.
The last three characters in Table 1 were studied in detail,
based on samples of two flowers per individual F2 plant,
taken before they were transplanted into the field — that
is, at a time when all plants were in a reasonably uniform
environment, and before nectar was removed by pollinators. About 95% of bee visits to the transplanted plants of
the parent species were by native bumblebees, and all
hummingbird visits were by Anna’s hummingbirds, very
similar to what is observed in natural populations of the
two plant species.
Based on more than 8,000 pollinator visits to 228 F2
plants, bee visitation rate was significantly negatively
correlated, and hummingbird visitation significantly positively correlated, with flower anthocyanin content. These
opposing effects show that anthocyanins contribute to
reproductive isolation (Figure 2). Interestingly, however,
other characters merely affected one kind of pollinator or
the other. Increased carotenoid content caused a reduction
in bee visits but did not increase visits by hummingbirds,
while nectar volume per flower increased hummingbird
visits without affecting bee visitation, and increased petal
area correlated only with bee visitation. Bee pollination is
Effects of several flower character differences on daily visitation rates
by bees and hummingbirds.
presumably the ancestral condition, and so it is interesting
that, unlike most Mimulus, which are yellow-flowered,
M. lewisii has pink flowers (perhaps making it easier to
evolve the red colour of M. cardinalis). Given that adaptation to a new pollinator is unlikely to occur in a single step,
the initial changes making flowers attractive to hummingbirds should thus be advantageous if hummingbirds are
common, but only if bee visitation is not greatly decreased.
This study provides a convincing case in which a set of
changes driven by natural selection have led to the
reproductive isolation of a pair of closely related populations (natural hybrids do not occur between the two
Mimulus species, see [11]). Although the order of the
evolutionary changes, and the nature of the change that
started the process of isolation, are still unknown, the
work has afforded an opportunity to dissect the genetic
basis of the traits involved, by a quantitative-trait
linkage (QTL) mapping study involving numerous molecular markers [10]. The carotenoid-content difference in
the upper petals of these two species is largely due to a
single major gene [11]. This difference alone significantly
affects bee visits; in F2 plants, homozygosity for the M.
cardinalis (recessive) allele for high carotenoid content
reduced bee visits by over 75%. It is intriguing that
increased carotenoid content was presumably disadvantageous until after the change to high anthocyanin (which
attracts hummingbirds). Schemske and Bradshaw [4] even
suggest that its advantage in M. cardinalis may have been
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to deter bees rather than to attract hummingbirds. It
would thus be very interesting to know how the different
flower colour characteristics interact in the effects on pollinators observed with the F2 plants.
For several other traits, there is also evidence for major
effects — defined as ≥25% of the species difference —
associated with individual molecular markers [10]. For
instance, a single molecular marker difference is associated with 41% of the parental difference in nectar
volume [10]. Tests on the F2 population showed that
this has a significant effect on visitation, this time by
hummingbirds only [4]. Schemske and Bradshaw [4]
provocatively suggest that their evidence for the involvement of major genes conflicts with neo-Darwinian orthodoxy that “adaptation and reproductive isolation are
caused by a nearly infinite number of mutations of individually small effect”.
The existence of such an orthodoxy is questionable,
however. Fisher’s [12] often cited proposition, that small
random mutational perturbations to a complex system are
much more likely to be selectively advantageous than
large ones, must be viewed in the context of his pioneering work on ecological genetics (with several collaborators), which utilized natural major gene polymorphisms to
study natural selection in the wild [13]. Indeed, much
classic work on the quantitative genetics of adaptive
differentiation between local populations of the same
species has been summed up as indicating contributions
from “a few loci with major effects though probably many
with minor ones” (page 365 in [14]).
As Wright pointed out in his review [15] of Goldschmidt’s
masterpiece of evolutionary heterodoxy [16] “The neoDarwinists have not been concerned primarily with ... the
types of mutation involved in evolution. Their primary
concern is the dynamics of the process, accepting all types
of mutation actually observed”. The critical distinction is
between the idea that complex differences between
species arise through a single “macromutational” change
affecting a whole set of traits simultaneously, as postulated
by Goldschmidt [16] and by some advocates of evolution
by punctuated equilibria [17], and the view that selection
works on individually advantageous changes affecting
separate traits [5]. The Mimulus case provides yet more
support for the latter viewpoint.
References
1. Dobzhansky T: Genetics and the Origin of Species. New York:
Columbia University Press; 1937.
2. Grant V: Modes and origins of mechanical and ethological
isolation in angiosperms. Proc Natl Acad Sci USA 1994, 91:3-10.
3. Waser NM: Pollination, angiosperm speciation, and the nature of
species boundaries. Oikos 1998, 82:198-201.
4. Schemske DW, Bradshaw HD: Pollinator preferences and the
evolution of floral traits in monkeyflowers (Mimulus). Proc Natl
Acad Sci USA 1999, 96:11910-11914.
5. Darwin CR: The Origin of Species. London: John Murray; 1859.
6. Darwin CR: The Various Contrivances by which Orchids are
Fertilised by Insects. London: John Murray; 1862.
7. Proctor MCF, Yeo PF: The Pollination of Flowers. London:
Collins; 1973.
8. Grant V: Floral isolation between ornithophilous and
sphingophilous species of Ipomopsis and Aquilegia. Proc Natl
Acad Sci USA 1992, 89:11828-11831.
9. Richards AJ: Plant Breeding Systems (2nd edn). London: George
Allen and Unwin; 1997.
10. Bradshaw HD, Otto SM, Frewen BE, McKay JK, Schemske DW:
Quantitative trait loci affecting differences in floral morphology
between two species of monkeyflower (Mimulus). Genetics 1998,
149:367-382.
11. Hiesey WM, Nobs MA, Björkman O: Experimental Studies on the
Nature of Species. V. Biosystematics, Genetics and Physiological
Ecology of the Euryanthe Section of Mimulus. Washington, D.C.:
Carnegie Institute of Washington; 1971.
12. Fisher RA: The Genetical Theory of Natural Selection. Oxford:
Clarendon Press; 1930.
13. Ford EB: Ecological Genetics (Fourth Edition). London: Chapman
and Hall; 1975.
14. Wright S: Evolution and the Genetics of Populations. Vol.4. Variability
Within and Between Populations. Chicago, Illinois: University of
Chicago Press; 1978.
15. Wright S: The material basis of evolution: a review. Sci Monthly
1941, 53:165-170.
16. Goldschmidt RB: The Material Basis of Evolution. New Haven,
Connecticut: Yale University Press; 1940.
17. Gould SJ: Is a new and general theory of evolution emerging?
Paleobiology 1980, 6:119-130.