The role of mate choice in biocomputation:
Sexual selection as a process of search, optimization, and
diversification
Geoffrey
Millers current address:
Psychology, Logan Hall 160
University of New Mexico
Albuquerque, NM 87131-1161, USA
(505) 277-1967 (office voice/fax)
(505) 277-1394 (dept fax)
http://www.unm.edu/~psych/faculty/gmiller.html
Peter Todds current address:
Center for Adaptive Behavior and
Cognition
Max Planck Institute for Human
Development
Lentzeallee 94
14195 Berlin, Germany
http://www-abc.mpib-berlin.mpg.de/users/ptodd/
Published in: W.
Banzof & F. H. Eeckman (Eds.) (1995). Evolution
and Biocomputation: Computational Models of Evolution. Lecture Notes in
Computer Science 899. (pp. 169-204). Springer-Verlag.
Abstract
The most successful, complex, and numerous species on earth
are composed of sexually-reproducing animals and flowering plants. Both groups typically undergo a form of
sexual selection through mate choice: animals are selected by conspecifics and
flowering plants are selected by heterospecific pollinators. This suggests that the evolution of
phenotypic complexity and diversity may be driven not simply by
natural-selective adaptation to econiches, but by subtle interactions between
natural selection and sexual selection.
This paper reviews several theoretical arguments and simulation results
in support of this view. Biological
interest in sexual selection has exploded in the last 15 years (see Andersson
& Bradbury, 1987; Cronin, 1991), but has not yet been integrated with the
biocomputational perspective on evolution as a process of search and
optimization (Holland, 1975; Goldberg, 1989).
In the terminology of sexual selection theory, mate preferences for
"viability indicators" (e.g.
Hamilton & Zuk, 1982) may enhance evolutionary optimization, and
mate preferences for "arbitrary traits" (e.g. Fisher, 1930) may enhance evolutionary
search and diversification.
Specifically, as a short-term optimization process, sexual selection
can: (1) speed evolution by increasing the accuracy of the mapping from
phenotype to fitness and thereby decreasing the "noise" or
"sampling error" characteristic of many forms of natural selection,
and (2) speed evolution by increasing the effective reproductive variance in a
population even when survival-relevant differences are minimal, thereby
imposing an automatic, emergent form of "fitness scaling", as used in
genetic algorithm optimization methods (see Goldberg, 1989). As a longer-term search process, sexual
selection can: (3) help populations escape from local ecological optima,
essentially by replacing genetic drift in Wright's (1932) "shifting
balance" model with a much more powerful and directional stochastic
process, and (4) facilitate the emergence of complex innovations, some of which
may eventually show some ecological utility.
Finally, as a process of diversification, sexual selection can (5)
promote spontaneous sympatric speciation through assortative mating, increasing
biodiversity and thereby increasing the number of reproductively isolated
lineages performing parallel evolutionary searches (Todd & Miller, 1991)
through an adaptive landscape. The net
result of these last three effects is that sexual selection may be to
macroevolution what genetic mutation is to microevolution: the prime source of
potentially adaptive heritable variation, at both the individual and species
levels. Thus, if evolution is understood
as a biocomputational process of search, optimization, and diversification,
sexual selection can play an important role complementary to that of natural
selection. In that role, sexual
selection may help explain precisely those phenomena that natural selection
finds troubling, such as the success of sexually-reproducing lineages, the
speed and robustness of evolutionary adaptation, and the origin of otherwise
puzzling evolutionary innovations, such as the human brain (Miller, 1993). Implications of this view will be discussed
for biology, psychology, and evolutionary approaches to artificial intelligence
and robotics.
Keywords: sexual
selection, mate choice, optimization, speciation, evolutionary innovation,
genetic algorithms, biodiversity
Introduction
Sexual selection through mate choice (Darwin, 1871) has
traditionally been considered a minor, peripheral, even pathological process,
tangential to the main work of natural selection and largely irrelevant to such
central issues in biology as speciation, the origin of evolutionary
innovations, and the optimization of complex adaptations (see Cronin,
1991). But this traditional view is at
odds with the fact that the most complex, diversified, and elaborated taxa on
earth are those in which mate choice operates: animals with nervous systems,
and flowering plants. The dominance of
these life-forms, and the maintenance of sexual reproduction itself, has often
been attributed to the advantages of genetic recombination. But recombination alone is not diagnostic of
animals and flowering plants: bacteria and non-flowering plants both do sexual
recombination. Rather, the interesting
common feature of animals and flowering plants is that both undergo a form of
sexual selection through mate choice.
Animals are sexually selected by opposite-sex conspecifics (Darwin,
1871; see Cronin, 1991), and flowering plants are sexually selected by
heterospecific pollinators such as insects and hummingbirds (Sprengel, 1793;
Darwin, 1862; see Barth, 1991). Indeed,
Darwin's dual fascination with animal courtship (Darwin, 1871) and with the
contrivances of flowers to attract pollinators (Darwin, 1862) may reflect his
understanding that these two phenomena shared some deep similarities.
The importance of mate choice in evolution can be
appreciated by considering the special properties of neural systems as
generators of selection forces. The
brains and sensory-motor systems of organisms make choices that affect the
survival and reproduction of other organisms in ways that are quite different
from the effects of inanimate selection forces (as first emphasized by Morgan,
1888). This sort of psychological
selection (Miller, 1993; Miller & Freyd, 1993) by animate agents can have
much more direct, accurate, focused, and striking results than simple
biological selection by ecological challenges such as unicellular parasites or
physical selection by habitat conditions such as temperature or humidity. Recently, several biologists have considered
the evolutionary implications of "sensory selection", perhaps the
simplest form of psychological selection (see Endler, 1992; Guilford &
Dawkins, 1991; Ryan, 1990; Ryan & Keddy-Hector, 1992). This paper emphasizes the evolutionary
effects of mate choice because mate choice is probably the strongest, most
common, and best-analyzed type of psychological selection. But there are many other forms of
psychological selection both within and between species. For example, the effects of psychological
selection on prey by predators results in mimicry, camouflage, warning
coloration, and protean (unpredictable) escape behavior. Artificial selection on other species by
humans, whether for economic or aesthetic purposes, is simply the most
self-conscious and systematic form of psychological selection. Thus, we can view sexual selection by
animals choosing mates as mid-way between brute natural selection by the
inanimate environment, and purposive artificial selection by humans.
But the big questions remain: What distinctive evolutionary
effects arise from psychological selection, and in particular from sexual
selection through mate choice? And how does sexual selection interact with
other selective forces arising from the ecological and physical environment?
The traditional answer has been that sexual selection either copies natural
selection pressures already present (e.g.
when animals choose high-viability mates) making it redundant and
impotent, or introduces new selection pressures irrelevant to the real work of
adapting to the econiche (e.g. when animals
choose highly ornamented mates), making it distracting and maladaptive. In this paper we take a more positive view
of sexual selection. By viewing
evolution as a "biocomputational" process of search, optimization,
and diversification in an adaptive landscape of possible phenotypic designs, we
can better appreciate the complementary roles played by sexual selection and
natural selection. We suggest that the
success of animals and flowering plants is no accident, but is due to the
complex interplay between the dynamics of sexually-selective mate choice and
the dynamics of naturally-selective ecological factors. Both processes together are capable of
generating complex adaptations and biodiversity much more efficiently than
either process alone. Mate choice can
therefore play a critical role in biocomputation, facilitating not only
short-term optimization within populations, but also the longer-term search for
new adaptive zones and new evolutionary innovations, and even speciation and
the macroevolution of biodiversity.
This paper begins with a discussion of the historical
origins of the idea of mate choice (section 2) and the evolutionary origins of
mate choice mechanisms (section 3). We
then explore how mate choice can improve biocomputation construed as adaptive
population movements on fitness landscapes, by allowing faster optimization to
fitness peaks (section 4), easier escape from local optima (section 5), and the
generation of evolutionary innovations (section 6). Moving from serial to parallel search, we then consider how
sexual selection can lead to sympatric speciation and thus to evolutionary
search by multiple independent lineages (section 7). Finally, section 8 discusses some implications of these ideas for
science (particularly biology and evolutionary psychology) and some
applications in engineering (particularly genetic algorithms research and
evolutionary optimization techniques).
This theoretical paper complements our earlier work on genetic algorithm
simulations of sexual selection (Miller, accepted, a; Miller & Todd, 1993;
Todd & Miller, 1991, 1993); in further work we will test these ideas with
more extensive simulations (Todd & Miller, in preparation) and comparative
biology research (Miller, accepted, b; Miller, 1993).
The evolution
of economic traits through natural selection versus the evolution of
reproductive traits through sexual selection
Darwin (1859, 1871) clearly distinguished between natural
selection and sexual selection as different kinds of processes operating on
different kinds of traits according to different kinds of evolutionary
dynamics. For him, natural selection
improved organisms' abilities to survive in an environment that is often
hostile and always competitive, while sexual selection honed abilities to
attract and select mates and to produce viable and attractive offspring. But this critical distinction between
natural and sexual selection was lost with the Modern Synthesis (Dobzhansky,
1937; Huxley, 1942; Mayr, 1942; Simpson, 1944), when natural selection was
redefined as any change in gene frequencies due to the fitness effects of
heritable traits, whether through differential survival or differential
reproduction. The theory of sexual
selection through mate choice had been widely dismissed after Darwin, and this
brute-force redefinition of natural selection to encompass virtually all
non-random evolutionary processes did nothing to revive interest in mate
choice.
Fisher (1915, 1930) was one of the few biologists of his era
to worry about the origins and effects of mate choice. He developed a theory of "runaway
sexual selection," in which an evolutionary positive-feedback loop is
established (via genetic linkage) between female preferences for certain male
traits, and the male traits themselves.
As a result, both the elaborateness of the traits and the extremity of
the preferences could increase at an exponential rate. Fisher's model could account for the wildly
exaggerated male traits seen in many species, such as the peacock's plumage,
but it did not explain the evolutionary origins of female preferences
themselves, and was not stated in formal genetic terms. Huxley (1938) criticized Fisher's model in a
hostile and confused review of sexual selection theory, which kept Darwin's
theory of mate choice in limbo for decades to come.
In the last 15 years, however, there has been an explosion
of work on sexual selection through mate choice. The new population genetics models of O'Donald (1980), Lande
(1981), and Kirkpatrick (1982) supported the mathematical feasibility of
Fisher's runaway sexual selection process.
Behavioral experiments on animals showed that females of many species do
exhibit strong preferences for certain male traits (e.g. Andersson, 1982; Catchpole, 1980; Ryan,
1985). New comparative morphology has
supported Darwin's (1871) claim that capricious elaboration is the hallmark of
sexual selection: for instance, Eberhard (1985) argued that the only feasible
explanation for the wildly complex and diverse male genitalia of many species is
evolution through female preference for certain kinds of genital
stimulation. Evolutionary computer
simulation models such as those of Collins and Jefferson (1992) and Miller and
Todd (1993) have confirmed the plausibility, robustness, and power of runaway
sexual selection. Once biologists
started taking the possibility of female choice seriously, evidence for its
existence and significance came quickly and ubiquitously. Cronin (1991) provides a readable,
comprehensive, and much more detailed account of this history.
Largely independently of this revival of sexual selection
theory, Eldredge (1985, 1986, 1989) has developed a general model of evolution
based on the interaction of a "geneological hierarchy" composed of
genes, organisms, species, and monophyletic taxa, and an "ecological
hierarchy" composed of organisms, "avatars" (sets of organisms
that each occupy the same ecological niche), and ecosystems. Phenotypes in this view are composed of two
kinds of traits: "economic traits" that arise through natural
selection to deal with the ecological hierarchy, and "reproductive
traits" that arise through sexual selection to deal with other entities
(e.g. potential mates) in the
geneological hierarchy. Eldredge (1989)
emphasizes that the relationship between economic success and reproductive
success can be quite weak, and that reproductive traits are legitimate
biological adaptations as shown by recent research on mate choice and
courtship displays (see Cronin, 1991).
Eldredge also grants geneological units their own hierarchy separate
from the ecological one, but does not emphasize the possibility of evolutionary
dynamics occurring entirely within the geneological hierarchy, without any
ecological relevance. The one exception
is Eldredge's discussion of how "specific mate recognition systems"
(SMRSs) might be disrupted through stochastic effects, resulting in spontaneous
speciation. But other processes
occurring purely within the geneological hierarchy, such as Fisher's (1930)
runaway process, are not mentioned.
Thus, even in his authoritative review of macroevolutionary theory
(Eldredge, 1989), which consistently views evolutionary change in terms of
movements through adaptive landscapes, Eldredge overlooks the adaptive autonomy
of sexual selection, and the adaptive interplay between sexual selection and
natural selection.
But the time is now right to take sexual selection seriously
in both roles: (1) as a potentially autonomous evolutionary process that can
operate entirely within Eldredge's "geneological hierarchy", and (2)
as a potentially important complement to natural selection that can facilitate
adaptation to Eldredge's "ecological hierarchy" in various ways. The remainder of this paper focuses on this
second role. But to understand the dynamic
interplay between natural and sexual selection, we must first understand their
different characteristic dynamics.
Natural selection typically results in convergent evolution
onto a few (locally) optimal solutions given pre-established problems posed by
the econiche. In natural selection by
the ecological niche or the physical habitat, organisms adapt to environments,
but not vice-versa (except in relatively rare cases of tight co-evolution see
Futuyama & Slatkin, 1983). This
causal flow of selection from environment to organism makes natural selection
fairly easy to study empirically and formally, because one can often identify a
relatively stable set of external conditions (i.e. a "fitness function") to which a species adapts. Moreover, natural selection itself is
primarily a hill-climbing process, good at exploiting adaptive peaks, but
somewhat weak at discovering them.
By contrast, sexual selection often results in an
unpredictable, divergent pattern of evolution, with lineages speciating spontaneously
and exploring the space of phenotypic possibilities according to their
capriciously evolved mate preferences.
In sexual selection, the mate choice mechanisms that constitute the
selective "environment" can themselves evolve under various forces,
including the current distribution of available phenotypes. Thus, the environment and the adaptations
the traits and preferences can co-evolve under sexual selection, as Fisher
(1930) realized. The causal flow of
sexual selection forces is bi-directional, and thus more complex and
chaotic. The resulting unpredictable
dynamics may look entirely anarchic, without structure and due entirely to
chance, but are in fact "autarchic", in that a species evolving
through strong selective mate choice is a self-governing system that in a sense
determines its own evolutionary trajectory.
Indeed, sexual selection could be considered the strongest form of
biological self-organization that operates apart from natural selection but
it is a form almost entirely overlooked by those who study self-organization
from a biocomputational perspective (see e.g.
Langton et al., 1993; Kauffman, 1993).
If one visualizes sexual selection dynamics as branching,
divergent patterns that explore phenotype space capriciously and autonomously,
and natural selection dynamics as convergent, hill-climbing patterns that seek
out adaptive peaks, then their potential complementarity can be
understood. The overall evolutionary
trajectory of a sexually-reproducing lineage results from the combined effects
of sexual selection dynamics and natural selection dynamics (plus the
stochastic effects of genetic drift and neutral drift) an interplay of
capriciously directed divergence and ecologically directed convergence. This interplay might help explain
evolutionary patterns that have proven difficult to explain under natural
selection alone, particularly the abilities of lineages to optimize complex
adaptations, to escape from local evolutionary optima, to generate evolutionary
innovations, and to split apart into sympatric species.
This interplay between capricious, divergent sexual
selection and natural selection is analogous to the interplay between genetic
mutation and natural selection. The
major difference is that the high-level variation in phenotypic design produced
by sexual selection is much richer, more complex, and typically less
deleterious than the low-level variation in protein structure produced by
random genetic mutation. Thus, many of
the phenomena that seem difficult to account for through the interaction of
low-level genetic mutation and natural selection, might be better accounted for
through the interaction of higher-level sexual-selective effects and natural
selection. But we should consider the
evolutionary origins of mate choice before we consider its evolutionary
effects.
Why mate
choice mechanisms evolve
Darwin (1871) analyzed the evolutionary effects but not the
evolutionary origins of mate preferences.
Fisher (1915, 1930) went further in discussing how mate preferences
might co-evolve with the traits they prefer, by becoming genetically linked to
them, but he too did not directly consider the selection pressures on mate
choice itself. Recently, the question
of how selective mate choice can evolve has occupied an increasingly important
position in sexual selection theory (e.g.
Bateson, 1983; Kirkpatrick, 1982, 1987; Pomiankowski, 1988; Sullivan,
1989); the issue becomes particularly acute when mate choice is costly in terms
of energy, time, or risk (Iwasa et al., 1991; Pomiankowski, 1987, 1990;
Pomiankowski et al., 1991).
The mysterious origins of mate choice can be made clearer if
the adaptive utility of choice in general is appreciated. Little sleep is lost over the issues of how
habitat choice, food choice, or nesting place choice could ever evolve given
their costs; the same acceptance ought to apply to mate choice. Animal nervous systems have two basic
functions: (1) generating adaptive survival behavior that registers, and
exploits or avoids, important objects and situations in the ecological
environment, such as food, water, prey, and predators (which we collectively
call "ecological affordances"), and (2) generating adaptive
reproductive behavior that registers and exploits important objects in the sexual
environment, such as viable, fertile, and attractive mates (which we
collectively call "reproductive affordances"). Current theories of how animals make
adaptive choices among ecological affordances are substantially more
sophisticated than theories of how animals make adaptive choices among
reproductive affordances. However, by
seeing both ecological affordances and reproductive affordances as examples of
"fitness affordances" in general (Miller & Freyd, 1993; Todd
& Wilson, 1993), we can see the underlying similarity between both sorts of
adaptive choice behavior. The key to
choosing food adaptively is to have evolved a food-choice mechanism that has
internalized the likely survival effects of eating different kinds of foods:
from an evolutionary perspective, the internally represented utility of a food
item should reflect its objectively likely prospective fitness effects on the
animal, given its energy requirements, biochemistry, gut morphology, etc. By analogy, the key to choosing mates
adaptively is to evolve a mate choice mechanism that has internalized the
likely long-term fitness consequences of reproducing with different kinds of
potential mates, given a certain recurring set of natural and sexual selection
pressures. The adaptive benefit of choice
in each case is that negative fitness affordances that threatened survival or
fertility in the past can be avoided, and positive fitness affordances that
enhanced survival or fertility in the past can be exploited. Thus, choice is a way of internalizing
ancestral selection pressures into current psychological mechanisms.
This view of the evolution of choice suggests that mate
choice mechanisms can be analyzed according to normative criteria of
adaptiveness. The internally
represented sexual attractiveness of a potential mate should reflect its
objectively likely prospective fitness value as a mate, in terms of the likely
viability and sexual attractiveness of any offspring that one might have with
it. Thus, the efficiency and
normativity of a mate choice mechanism could in principle be assessed with the
same theoretical rigor as a mechanism for any other kind of adaptive
choice. Mate choice is well-calibrated
if the perceived sexual attractiveness of potential mates is highly correlated
with the actual viability, fertility, and attractiveness of the offspring they
would produce. The observable traits of
potential mates that correlate primarily with offspring survival prospects can
be termed "viability indicators" (Zahavi, 1975), and the observable
traits that correlate primarily with offspring reproductive prospects can be
called "aesthetic courtship displays" of the sort analyzed by Darwin
(1871) and Fisher (1930). In fact, most
sexually-elaborated traits such as the peacock's tail will probably play both
roles to some extent, with their large costs making them useful viability
indicators (e.g. Petrie, 1992) but the
details of their design making them attractive aesthetic displays (e.g. Petrie et al., 1991).
Now we can ask, what actually gets "evolutionarily
internalized" from the environment (Shepard, 1984, 1987) in the case of
mate preferences? Mate choice mechanisms may in some cases evolve to
"represent" the recent history of a population's evolutionary
trajectory through phenotype space, that is, the recent history of natural
selection and sexual selection patterns that have been operating in the
population. Sustained, directional
movement through phenotype space typically implies that directional selection
is operating, or that a fitness gradient is being climbed in a certain
direction. Mate preferences which are
in agreement with this directional movement, internalizing the species' recent
history, will then be more successful, assuming the movement continues. In this case, mate preferences can be
described as "anticipatory" assessments of past selection pressures
that will probably continue to be applied in the future, in particular to one's
offspring.
This picture of how mate preferences evolve has clear
implications for sexual-selection dynamics.
If a population has not been moving through phenotypic space, e.g. it is perched atop an adaptive peak due to
stabilizing selection, as most populations are most of the time, then mate
preferences will probably evolve to favor potential mates near the current
peak, and they will tend to reinforce the stabilizing natural selection that is
currently in force. (If biased mutation
tends to displace individuals from the peak more often in one direction than in
another, then mate preferences may evolve to counteract that recurrent
deleterious mutation by having a directional component see Pomiankowski et
al., 1991.) But if a population has been evolving and moving through phenotype
space, then mate preferences can evolve to "point" in the direction
of movement, conferring more evolutionary "momentum" on the
population that it would have under natural selection alone. These sorts of directional mate preferences
(Kirkpatrick, 1987; Miller & Todd, 1993) can be visualized as momentum
vectors in phenotype space that can keep populations moving along a certain
trajectory, in some cases even after natural-selective forces have shifted.
Another effect could be seen when a population has been
splitting apart due to sympatric or allopatric divergence. In this case, mate preferences in each
sub-population can evolve to favor breeding within the sub-population, and not
between sub-populations, thereby reinforcing the speciation. The divergent mate preferences of two populations
splitting apart can be visualized as vectors pointing in different
directions. These sexual-selective
vectors will reinforce and amplify the initial effects of divergence by
imposing disruptive (sexual) selection against individuals positioned
phenotypically in between the parting populations. Thus, directional mate preferences will often evolve to be
congruent with whatever directional natural selection (if any) is operating on
a population, whether it applies to a unified population or one splitting apart
into subspecies. Sexual selection may
thereby smooth out and reinforce the effects of natural selection.
But sexual selection vectors can often point in different
directions from natural-selection vectors, resulting in a complex evolutionary
interplay between these forces. The evolution
of mate preferences can be influenced by a number of factors other than natural
selection for mate preferences in favor of high-viability traits. For example, stochastic genetic drift can
act on mate preferences as it can act on any phenotypic trait; this effect is
important in facilitating spontaneous speciation and in the capriciousness of
runaway sexual selection. Intrinsic
sensory biases in favor of certain kinds of courtship displays, such as louder
calls or brighter colors, may affect the direction of sexual selection (Endler,
1992; Guilford & Dawkins, 1991; Ryan, 1990; Ryan & Keddy-Hector,
1992). Also, an intrinsic psychological
preference for novelty, as noted by Darwin (1871) and in work on the
"Coolidge effect" (Dewsbury, 1981), may favor low-frequency traits
and exert "apostatic selection" (Clarke, 1962), a kind of centrifugal
selection that can maintain stable polymorphisms, facilitate speciation, and
hasten the evolution of biodiversity.
Thus, a number of effects may lead mate choice mechanisms to diverge
from preferring the objectively highest-viability mate as the sexiest
mate. These effects will often make
sexual-selective vectors diverge from natural-selective gradients in phenotype
space, and give sexual selection its capricious, divergent, unpredictable
nature. Now that we have considered the
evolutionary origins of mate preferences, we can consider their evolutionary
effects.
Ecological
optimization can be facilitated by selective mate choice
Natural selection is often analyzed theoretically, and
implemented computationally, as a more or less simple "fitness
function" that maps from phenotypic traits to reproductive success scores
(Goldberg, 1989). But natural selection
as it actually operates in the wild is often a horribly noisy, irregular, and
inaccurate process. Predators might
often eat the prey animal that has the better vision, larger brain, and longer
legs, simply because that animal happened to be closer at dinner time than the
duller, blinder, slower animal over the hill.
A lethal virus may attack and eliminate the animal with the better
immune system simply because that animal happened to drink from the wrong
pond. Anyone who doubts the noisiness
and inaccuracy of natural selection should consider the relative speed at which
animals evolve in the wild versus under artificial selection by human breeders,
who cull undesirable traits with much more accuracy and thoroughness. Maynard Smith (1978, p. 12) observed that evolution can happen up to
five orders of magnitude (100,000 times) faster under artificial selection than
under typical natural selection, at least over the short term.
The fundamental reason for this disparity is that Nature
(i.e. the physical habitat or
biological econiche) has no incentive to maximize the selective efficiency or
accuracy of natural selection, whereas human breeders do have incentives to
maximize the efficiency and accuracy of artificial selection. Likewise, animals choosing mates have very heavy
incentives to maximize the efficiency and accuracy of their mate choice, and
thereby the efficiency and accuracy of the sexual selection that they
impose. Thus, it would be extremely
surprising if the selective efficiency and accuracy of natural selection were
typically as high as that of sexual selection through mate choice. Habitats and econiches are not well-adapted
to impose natural selection, whereas animals are well-adapted to choose mates
and thereby to impose sexual selection.
(This difference is often obscured in genetic algorithms research, where
fitness functions are specifically designed by humans to be efficient and
accurate selectors.)
Given the relative noisiness and inefficiency of natural
selection itself, how did the "organs of extreme perfection and
complication" that Darwin (1859) so admired ever manage to evolve? We
believe they do so with substantial assistance from selective mate choice, at
least in animals and flowering plants.
As we saw in the previous section, sexually reproducing animals have
strong incentives to internalize whatever natural-selection pressures are being
applied to their population in the form of selective mate preferences. For example, these preferences can inhibit
mating with individuals that probably survived by luck rather than by genetic
merit, whatever genetic merit means given current natural-selective and
sexual-selective pressures. By avoiding
mates that have low apparent viability but happen to still be alive anyway,
parents can keep from having offspring that would probably not be so lucky. Conversely, by mating with individuals who
clearly show high viability and sexual attractiveness, parents may give their
offspring a genetic boost with respect to natural and sexual selection for
generations to come. For example, an
average individual who mates with someone with twice their viability or
attractiveness may increase their long-term reproductive success (e.g. number of surviving grand-children) by
roughly 50% compared to random mating, by having their genes
"hitch-hike" in bodies with the better genes of their mate. This inheritance of genetic and economic
advantage through mate choice can have several important effects on the
optimization of complex adaptations, because the brains and sensory systems
involved in mate choice can act as highly efficient "lenses" for
reflecting, refracting, recombining, amplifying, and focusing natural selection
pressures.
First, the noisiness of natural selection can be
substantially reduced by mate choice, leading to smoother, faster evolutionary
optimization. It might take a while for
mate preferences to accurately internalize the current regime of natural
selection, but once in place, such preferences can exert much more accurate,
less noisy selection than natural selection itself can. For example, natural selection by viruses
alone (a biological selector) might yield a low correlation between heritable
immune system quality and reproductive success, because the infected animals
might be too sick to have a full-sized litter, but still manage to have several
offspring despite their illness. But
mate choice based on observed health and immune capacity may boost this
correlation much higher, if conspecifics refuse to mate at all with an
individual who bears the viral infection, and thereby lower the sick
individual's reproductive success to nil.
The higher the correlation between heritable phenotypic traits and
reproductive success, the faster the evolution (Fisher, 1930). Mate choice can therefore heavily penalize
individuals who show a tendency to get sick, whereas natural selection heavily
penalizes only those individuals who actually have fewer offspring or die. Here, the brains and sensory systems
involved in mate choice act to focus the noisy, diffuse, unreliable forces of
natural selection into smoother, steeper gradients of sexual selection. Thus, much of the work of constructing and
optimizing complex adaptations may be performed by mate choice mechanisms tuned
to reflect natural-selection pressures, rather than by the natural-selection
pressures themselves.
Of course, most animals that fail to reproduce especially
in r-selected species that produce large numbers of offspring with little
parental care will do so because they were spontaneously aborted, failed to
hatch, or died before reproductive maturity due to illness, starvation, or
predation. Out of the countless eggs
and sperm that adult salmon release during mating, only a very few zygotes will
survive the rigors of childhood and up-river migration to successfully choose
mates and spawn themselves. Natural
selection may eliminate almost all of the individuals in a particular
generation in this way. As Darwin
(1859) noted in his discussion of the inevitability of competition, the
manifest capability of organisms to reproduce far outstrips the carrying
capacity of their environment, so natural selection will eliminate the vast
majority of individuals. In contrast,
even the most intensive mate choice in highly polygynous species will not cull the
remaining reproductively-mature individuals from the mating game with anything
like this kind of ferocious efficiency.
A large number of bachelor males may not leave behind any offspring, but
most of the females and a significant number of males will, making sexual
selection look like a much weaker force in terms of the percentages of
individuals affected. But the
efficiency of a selective process depends most heavily on the correlation
between heritable phenotypic features and selective outcomes. In natural selection, this correlation may often
be quite low, because, as stressed earlier, Nature typically has no incentive
to increase its selective efficiency.
By contrast, this correlation may be quite high in sexual selection,
because animals have large incentives to increase their mate-choice
efficiency. Thus, although sexual
selection typically affects fewer individuals per generation than natural
selection, sexual selection may account for most of the nonrandom change in
heritable phenotypic traits i.e. most
of the evolution.
Second, mate choice can magnify relative fitness
differences, thereby increasing the speed and robustness of optimization. In genetic algorithms research, populations
often converge to have nearly similar performance on the objective fitness
function after a few dozen generations, and further optimization becomes
difficult because the relatively small fitness differences are insufficient to
result in much evolution. Methods for
"fitness scaling" such as linear rescaling or rank-based selection
can overcome this problem by mapping from small differences in objective
fitness (corresponding to ecological success) onto large differences in
reproductive success (Goldberg, 1989).
We believe that in nature, sexual selection can provide an automatic
form of fitness scaling that helps populations avoid this sort of evolutionary
stagnation. Again, sexually reproducing
animals have incentives to register slight differences in the observed
viability of potential mates and to mate selectively with higher-viability
individuals. The result of this
choosiness will be automatic fitness scaling that maintains substantial
variance in reproductive success and thereby keeps evolution humming along even
when every individual is similar in fitness (e.g. when near some optimum).
Here, brains and sensory systems act through the categorizing power of
mate choice so as to magnify small fitness differences, effectively separating
individuals who would otherwise have indistinguishable fitnesses (and have the
same number of offspring) into different distinguishable fitnesses and
thereby greatly increasing the variance in the number of offspring.
Third, mate choice mechanisms can pick out phenotypic traits
that are different from those on which natural selection itself acts, but that
are highly correlated with natural-selective fitness. For example, bilateral symmetry may be an important correlate of
ecological success for many vertebrates.
But natural selection might increase the degree of symmetry in a
particular lineage only very indirectly through its effects on several
different correlates of symmetry, such as locomotive efficiency (individuals
with asymmetric legs won't be able to get around as well and so will be
selected against on the grounds of their locomotive inefficiency, rather than
being selected against for asymmetry per se).
By contrast, mate preferences for perceivable facial and bodily form can
directly select for symmetry in a way that natural selection cannot. [1]. In general, mate choice can complement
natural selection by operating on perceivable phenotypic attributes that
underlay a wide array of economic traits, but which would typically be shaped
only indirectly by a number of different, weak, indirect natural selection
pressures. To continue our analogy
between brains and optical devices, mate choice mechanisms can act as panoramic
lenses, bringing into view a wider array of phenotypic features than natural
selection alone would tend to focus on.
Natural selection is extremely efficient at eliminating
major genetic blunders, such as highly deleterious mutations or disruptive
chromosome duplications it simply prevents the afflicted individual from
reaching reproductive maturity. But the
more subtle task of shaping and optimizing complex adaptations may be more difficult
for direct ecological selection pressures to manage. Natural selection alone can of course accomplish wonderful
things, given enough time: 3.5 billion years of prokaryote evolution (amounting
to many trillions of generations) has produced some quite intricate biochemical
adaptations in these single-celled organisms.
But for larger-bodied animals with slower generation times, we believe
that selective mate choice plays a major role in the optimization of complex
adaptations. For such species, the
efficacy of natural selection may depend strongly on shaping the mate choice
mechanisms that "take over" via sexual selection and do much of the
difficult evolutionary work.
There is suggestive data that support this claim. Bateson (1988) replotted data from Wyles,
Kunkel, and Wilson (1983), and found a strong positive correlation across
several taxa between rate of evolution (assessed by a measure of morphological
variability across eight traits) and relative brain size (see Figure 1). For example, song birds have larger brains
than non-song birds, and apparently evolve faster; humans have the largest
brains of all primates, and apparently evolve the fastest. Bateson (1988) interpreted this correlation
in terms of larger brains allowing better habitat choice, a stronger
"Baldwin effect" (in which the ability to learn actually speeds up
the evolution of unlearned traits see Hinton and Nowlan, 1987), and various
forms of "behaviorally induced environmental change" but he
overlooked the potential effects of brain size on sexual selection
patterns. We believe it is more
important that larger brains allow more powerful and subtle forms of selective
mate choice. Indeed, the vastly
enlarged human brain has allowed us not only to (unconsciously) impose strong
sexual selection on members of our own species (Darwin, 1871; Miller, 1993),
but also to impose very strong artificial selection on members of other species
(Darwin, 1859). The correlation between
brain size and rate of evolution provides a suggestive start for studies of the
relationship between the capacity for selective mate choice and the rate and
course of evolution, but clearly much more data is needed on this issue
Escaping
evolutionary local optima through sexual selection .
Escaping
local optima: The relative power of "sexual-selective drift", genetic
drift, and neutral drift
Populations can become perched on some adaptive peak in the
fitness landscape through the optimizing effect of sexual and natural selection
acting together. But many such peaks
are only local evolutionary optima, and better peaks may exist elsewhere. Once a population has converged on such a
locally optimal peak then, how can it move off that peak, incurring a temporary
ecological fitness cost, to explore the surrounding adaptive landscape and
perhaps find a higher-fitness peak elsewhere? Wright's (1932, 1982)
"shifting balance" theory was designed to address this problem of
escaping from local evolutionary optima.
He suggested that genetic drift operating in quasi-isolated populations
can sometimes allow one population to move far enough away from its current
fitness peak that it enters a new adaptive zone at the base of a new and higher
fitness peak. Once that population starts
to climb the new fitness peak, its genes can spread to other populations, so
that the evolutionary innovations involved in climbing this peak can eventually
reach fixation throughout the species.
Thus, the species as a whole can climb from a lower peak to a higher
one.
Wright's (1932) model anticipated some of the recent
concerns about how to take "adaptive walks" that escape from local
optima in rugged fitness landscapes (Kaufmann, 1993). In very rugged landscapes, short steps (defined relative to the
landscape's ruggedness) of the sort generated by genetic point mutations are
unlikely to allow individuals or populations to escape a local optimum. This is similar to Darwin's (1883) problem
of how minor mutations can accumulate into useful adaptations if they have no
utility in their initial form. But
jumping further across the landscape does not guarantee success, either: longer
steps of the sort generated by macromutations (as favored by Goldschmidt, 1940)
are unlikely to end up anywhere very reasonable; most mutations are
deleterious, and major mutations even more so.
The central problem is to make the "foray length" of
population movements away from local optima able to exploit the
"correlation length" of the adaptive landscape, and allow directional
excursions away from the current adaptive peak to explore the surrounding
fitness landscape. Wright's shifting
balance model suggests that genetic drift might provide enough random jiggling
around the local optimum to sometimes knock the population over into another
adaptive zone, but the analysis of adaptive walks in rugged fitness landscapes
(Kaufmann, 1993) indicates that this is unlikely to be a common occurrence.
Our model of population movement in phenotype space via mate
choice is similar to Wright's shifting balance theory, but it provides a
mechanism for exploring the local adaptive landscape that can be much more
powerful and directional than random genetic drift: sexual selection. Here, we are relying on a kind of
"sexual-selective drift" resulting from the stochastic dynamics of
mate choice and runaway sexual selection, to displace populations from local
optima. We suspect that with mate
choice, the effects of sexual-selective drift will almost always be stronger
and more directional than simple genetic drift for a given population size, and
will be more likely to take a population down from a local optimum and over
into a new adaptive zone. Genetic drift
relies on passive sampling error to move populations down from economic
adaptive peaks, whereas sexual selection relies on active mate choice, which
can overwhelm even quite strong ecological selection pressures. Our simulations have shown that with
directional mate preferences in particular, populations move around through
phenotype space much more quickly than they would under genetic drift alone
(Miller & Todd, 1993). Thus, sexual
selection can be seen as a way of making Wright's shifting balance model much
more powerful, by allowing active mate choice dynamics to replace passive genetic
drift as the main source of evolutionary innovation.
Aside from classical genetic drift (sampling error in small
populations), "neutral drift" through adaptively neutral mutations
(Kimura, 1983) might conceivably play an important role in allowing populations
to explore high-dimensional adaptive landscapes. The idea is this: the more dimensions there are to an adaptive
landscape, the less problematic local optima will be, because the more
equal-fitness "ridges" there will be from one optimum to another in
the space. A local optimum may be a
peak with respect to each of two phenotypic dimensions, but it is unlikely to
be a peak with respect to each of a thousand dimensions, so there will be
plenty of room for adaptively neutral exploration of phenotype space (see
Eigen, 1992; Schuster, 1988). Under
this model, populations can drift around through adaptive landscapes without
incurring fitness costs for doing the exploration.
The neutral drift theory is usually applied to molecular
evolution (DNA base pair substitutions typically do not change expressed
protein functionality), but it could in principle extend to morphology and
behavior. For example, if
quadrupedalism and bipedalism happen to have equal locomotive efficiency in a
certain environment (such as the Pleistocene savanna of Africa), a population
might drift from the former to the latter without incurring much fitness cost
in between, and without natural selection in favor of bipedalism per se.
Although both ways of moving may be equal in locomotive efficiency, they have
very different implications with respect to other potential activities such as
tool use. Once the population drifts
into bipedalism, it will happen to enter a new adaptive zone wherein natural
selection can favor new adaptations for tool use, resulting in an evolutionary
innovation with respect to tool use.
Thus, if the problem of local optima in high-dimensional adaptive
landscapes really is over-stated, then neutral drift from one adaptive zone to
another might facilitate the discovery of evolutionary innovations associated
with different adaptive peaks.
However, we believe that for complex phenotypic adaptations
at the level of morphology and behavior, the problems of local optima are not
so easily overcome. The evolutionary
conservatism characteristic of many morphological and behavioral traits in many
taxa suggests that neutral drift has trouble operating on such traits. Still, so little is known about neutral
drift above the level of molecules that such arguments are not convincing. We can however ask, if neutral drift theory
does apply to complex phenotypic traits, is neutral drift through phenotype
space likely to be faster with or without the capricious dynamics of sexual
selection? Here again, we believe that populations capable of mate choice are
more likely to move along fitness ridges and exploit the possibilities of
neutral drift, because mate choice can confer more mobility and momentum on
evolving populations
The role
of sexual dimorphism in escaping local optima through sexual selection
As Darwin (1871) noted, females are often choosier than
males about their mates, so sexual selection often acts more strongly on
males. Sexually dimorphic selection
pressures will often result in sexually dimorphic traits, although dimorphism
in a trait tends to evolve much more slowly than the trait itself (Lande, 1980,
1987). Thus, Darwin was able to use
sexual dimorphism as a diagnostic feature for a trait having evolved through
sexual selection. But the effects of
sexual dimorphism on longer-term evolutionary processes have rarely been
considered.
Highly elaborated male courtship displays, whether
behavioral or morphological, are often costly in terms of the male's
"economic" success with respect to the surrounding econiche. Indeed, according to Zahavi's (1975)
handicap theory, this cost is indirectly the reason why elaborated displays can
evolve under sexual selection. If we
view a dimorphic population as situated in an adaptive landscape that
represents purely ecological (economic) fitness, then the females will be
situated close to the fitness peak, while the males will be situated some
distance from the peak, and thus lower on the fitness landscape. As the male displays become more elaborated
and more costly, the males will travel further away from the fitness peak that
represents economic optimality.
Thus, sexual dimorphism in courtship traits leads to a kind
of sexual division of labor with respect to the job of exploring adaptive
landscapes. Males get pushed off
economic fitness peaks by the pressure of female choice in favor of highly
elaborated, costly courtship displays.
Due to the typical lack of male choosiness, the females can stay more
comfortably situated near the economic fitness peak. Thus, males become the explorers of the adaptive landscape,
compelled to wander through the space of possible phenotypic designs by the
demands of female choice to "bring home" a sexy, interesting, and
expensive courtship display. The
economic costs of wandering through phenotype space are compensated for by the
reproductive benefits of attracting mates with a costly, elaborated courtship
display. In most species most of the
time, the males will reach some equilibrium distance (Fisher, 1930;
Kirkpatrick, 1982), close enough to the economic fitness peak to survive, but
far enough away to demonstrate their viability and to incur the costs of an
elaborate display, and the species will be recognized as having some sexually
dimorphic traits.
But sometimes, in some species, the males might stumble upon
a new adaptive zone in the course of their wanderings. That is, a sexually-elaborated trait, or
some phenotypic side-effect of it, could prove economically useful, and would
be subject to favorable natural selection.
The males would then start to climb the new economic fitness peak; and
once the males reach a level of economic benefit on this new peak that exceeds
the benefit obtainable on the old fitness peak, then there can be selection for
females as well to move from their position on the old peak to the new, higher,
peak. This selection on females would
act to eliminate the sexual dimorphism that maintains the useful new traits in
the males alone, so that the females too could inherit the new trait (from
their fathers initially). Thus, once
the males enter a new adaptive zone and start to climb a higher fitness peak, a
combination of natural selection and reduced sexual dimorphism may move the
entire population, males and females, to the top of the new fitness peak. Populations that successfully shift from one
adaptive peak to another will show little sexual dimorphism for the original
courtship traits that brought them into the region of the new peak, since
selection on the females will have worked to remove it; instead, they will be
recognized as beneficiaries of an evolutionary innovation characteristic of
both males and females. So it may be
difficult to recognize modern species that have undergone this peak-jumping
process except through careful analysis of the fossil record; computer
simulation may be more useful in determining whether this peak-jumping
mechanism is plausible (see Todd & Miller, in preparation).
This possibly rapid shift between fitness peaks resembles
what Simpson (1944) called "quantum evolution" or what Eldredge and
Gould (1972) called a "punctuation".
The quantum evolution term is apt because our theory suggests that
populations capable of sexual dimorphism can do a kind of "quantum
tunneling" between adaptive peaks: the normal economic costs that slow
movement across low-fitness valleys between peaks can be over-ridden by
geneological (sexually selected) benefits to the males, allowing them to
traverse the valleys much more quickly.
The females can then join the males once a new peak is actually discovered. The result could be much more rapid movement
between peaks than would be possible under natural selection alone.
This rapid tunneling between peaks looks strange from the
perspective of the purely economic adaptive landscape that represents only
natural selection pressures. But that
landscape is not the whole picture: the effects of sexual selection establish a
separate "reproductive landscape" with different dimensions and
perhaps a different topography for males and females. The economic and reproductive landscapes together combine to form
a master adaptive landscape; what looks like paradoxical downhill movement or
quantum tunneling in the purely economic landscape traversed by natural
selection may actually be hillclimbing in the combined landscape that includes
sexual selection pressures.
But won't these initially economically-unfeasible excursions
by the males threaten their survival, and hence that of the species as a whole?
Sexual selection is often maligned for just this reason, as "a fascinating
example of how selection may proceed without adaptation" (Futuyma, 1986,
p. 278), on the principle that the
economic costs of highly elaborated male courtship displays might predispose a
species to extinction e.g. as argued
by Haldane (1932), Huxley (1938), and Kirkpatrick (1982). But as Pomiankowski (1988) has emphasized,
the relationship between male economic success and population viability is
quite complex and unclear. Reproductive
output in sexually-reproducing species is typically limited by the number of
females, not by the number of males.
The population's rate of replacement will not necessarily be decreased
by the loss of male viability due to elaborated courtship displays. On the contrary: "a population denuded
of males will have more resources available for females and so may support an
absolutely larger reproductive output for a given resource base"
(Pomiankowski, 1988). Thus, the
population-level costs of sexually-elaborated traits may be minimal, and the
individual-level benefits may be large, due to sexual selection. This makes quantum tunneling between
adaptive peaks through sexual selection a plausible mechanism for generating
evolutionary innovations and escaping local ecological optima.
At first glance, our proposal bears an uncomfortable
resemblance to traditional sexist images of males going out to hunt and
sometimes returning with meat for the benefit of their families. But females may also do some important
exploration of the adaptive landscape, with respect to different phenotypic
dimensions. Under Fisher's (1930)
runaway selection model for example, female preferences and male traits both
become elaborated through sexual selection.
Females become ever-choosier and more discriminating. The benefits of selective mate choice can
favor the evolution of new sensory, perceptual, and decision-making adaptations
in females, despite their economic costs.
Thus, while males are exploring the space of possible secondary sexual
characteristics and behavioral courtship displays under sexual selection,
females may be exploring the space of possible sensory, perceptual, and
cognitive traits. If the females happen
upon a mate choice mechanism such as a new form of color vision or better
timbre perception that also happens to have economic benefits in their
econiche, then we would expect such mechanisms to be further modified and
elaborated through natural selection, and inherited by males also, eventually
showing low dimorphism. Thus, females
can also tunnel between peaks in the space of possible perceptual systems,
deriving the reproductive benefits of selective mate choice even when a
perceptual system shows little ecological benefit.
In summary, sexual selection provides the easiest, fastest,
and most efficient way for populations to escape local ecological optima. Sexual dimorphism with respect to courtship
traits and mate preferences allows a sexual division of labor in searching the
adaptive landscape. Many morphological
and behavioral innovations that currently show economic utility and low sexual
dimorphism may have originated as parts of male courtship displays. Likewise, many sensory, perceptual, and
decision-making innovations could have originated as components of female
choice mechanisms, and later have been modified for ecological
applications. Those innovations that
did not happen to show any ecological utility remained in their sexually
dimorphic form, and are typically not recognized as innovations at all.
Sexual
selection and evolutionary innovations
The
mystery of evolutionary innovations
Evolutionary innovations are important because natural
selection crafts adaptations out of innovations: "Innovation is the
mainspring of evolution" (Jablonski & Bottjer, 1990, p. 253).
Classic examples of major evolutionary innovations include the bony
skeleton of vertebrates, the jaws of gnathostomes, the amniote egg, feathers,
continuously growing incisors, large brains in hominids, the insect wing, and
insect pollination of angiosperms (Cracraft, 1990). But the complete list of major evolutionary innovations is almost
endless, being virtually synonymous with the diagnostic characters of all
successful higher taxa, and the complete list of minor innovations would
include essentially all diagnostic characters of all species.
But, for all their biological importance and large number,
the causal origins of evolutionary innovations have been long contended and
remain poorly understood. Virtually
every major evolutionary theorist has tackled the problem of evolutionary
innovations, e.g. Darwin (1859, 1871,
1883), Romanes (1897), Weismann (1917), Wright (1932, 1982), Simpson (1953),
Mayr (1954, 1960, 1963), and Gould (1977).
But the major questions remain unresolved (see Nitecki, 1990, for a
recent review). This section reviews
the history of evolutionary thinking about innovations; section 6.2 examines
the most baffling features of innovations; section 6.3 suggests that sexual
selection through mate choice can help explain the strange pattern of
innovations in animals and flowering plants; section 6.4 outlines some limits
to our hypothesis; and section 6.5 concludes the discussion of innovations.
Darwin, particularly in the sixth edition of the Origin of
species (Darwin, 1883), worried about the early evolutionary stages of
"organs of extreme perfection" such as the human eye and the bird's
wing. How could these innovations be
preserved and elaborated before they could possibly assume their later survival
function (such as vision or flight)? The problem for Darwin was to account for
the origin of phenotypic innovation that was more complex and well-integrated
than what random mutation could produce, but that was not yet useful enough in
the struggle for existence to have been favored by natural selection. Mutations seemed able to generate only trivial
or disastrous phenotypic changes, so could not account for the origins of
useful innovations, whereas natural selection could only optimize innovations
already in place. Nor could Darwin
convince skeptics that some mysterious interplay between mutation and selection
could account for evolutionary innovations.
Darwin's difficulty in accounting for evolutionary
innovations was one of the weakest and most often-attacked aspects of his
theory of natural selection. Even his
most ardent followers were anxious about this problem. Romanes (1897) was very concerned to show
how "adaptive characters", or evolutionary novelties, originate. For him, this was the central question of
evolutionary theory, much more important than the question of how species
originate, but one that he was never
able to answer to his own satisfaction.
Simpson (1953) later proposed that "key mutations" can cause a
lineage to enter a new "adaptive zone" such that the lineage
undergoes an adaptive radiation, splitting apart into a large number of species
to exploit all the ecological opportunities in that new adaptive zone. Similarly, Mayr (1963) defined an
evolutionary innovation as "any newly acquired structure or property that
permits the performance of a new function, which, in turn, will open a new
adaptive zone" (Mayr, 1963, p.
602). However, both Simpson and
Mayr were better able to describe innovation's effects than to explain its
causes. Their notion that major
innovations are closely associated with adaptive radiations has been a
persistent theme in innovation theory, appearing more recently under the guise
of "key evolutionary innovations" in Liem (1973, 1990), and "key
characters" in Van Valen (1971).
Over this long history, several kinds of explanations have
been offered to explain the emergence of evolutionary innovations. Goldschmidt (1940) suggested that
macromutations could produce fully functioning novelties in the form of
"hopeful monsters". The
problem is that random macromutations are overwhelmingly unlikely to generate
the sort of structural complexity and integration characteristic of innovations
even in their early stages. Complex
innovations cannot be explained by undirected random mutation. On the other hand, Fisher (1930) took the
Darwinian hard line and maintained that innovations could indeed be produced
purely through natural-selective hill-climbing. The difficulty with this view is that it ignores the problem of
local optima, as discussed in section 5.
Significant innovation corresponds to fairly substantial movement
through a multi-dimensional adaptive landscape. But because many adaptive landscapes have complex structures
(Eigen, 1992; Kauffman, 1993), with many peaks, ridges, valleys, and local
optima, long movements through such landscapes may often require escaping from
local optima. As section 5.1
emphasized, this problem of escaping local optima is probably more serious at
the level of complex phenotypic design than at the level of genetic sequences
or protein shapes (cf. Eigen, 1992)
and most evolutionary innovations of interest to biologists are innovations in
complex phenotypic design. Thus, the
evolution of a new phenotypic innovation may often reflect escape from a local
adaptive optimum and the discovery of a better solution elsewhere in the space
of possible phenotypes (Wright, 1932; Patterson, 1988). Finally, other theorists have stressed the
role of phenotypic structure in allowing for innovations, through phenotypic
by-products of other adaptive change (Mayr, 1963), through various mechanisms
of phenotypic self-organization (e.g.
Eigen, 1992; Kauffman, 1993), and through changes in developmental
mechanisms, particularly "heterochronies" that affect the relative
timing of the development of different traits (Bonner, 1982; Goodwin et al.,
1983; Gould, 1977; Muller, 1990; Raff, 1990; Raff & Raff, 1987). These sorts of phenotypic constraints and
correlations are probably important, but as we will see, they cannot explain
the most striking features of the distribution of evolutionary innovation. There are three major problems for these
traditional theories about evolutionary innovation; these will be examined in
turn.
Three
puzzling aspects of evolutionary innovation
First, there is a disparity between the huge number of minor
varietal innovations and the small number of ecologically useful
innovations. Darwin (1883, p. 156) stressed this problem when he quoted
Milne Edwards: "Nature is prodigal in variety but niggardly in
innovation. Why ... should there be so much variety and so
little real novelty?". The vast
majority of characteristic innovations are "inconsequential" (Liem,
1990); they are what Francis Bacon called "the mere Sport of Nature"
when he disparaged the apparently pointless variety of animals, plants, and
fossils (quoted in Cook, 1991.) Only very few of the initially inconsequential
minor innovations may lead to major innovative evolutionary shifts in form or
function that allow the invasion of major new habitats and adaptive zones. But if evolutionary innovations spread
through populations under the influence of traditional natural selection for
their ecological utility, why do so few innovations show the sort of ecological
utility that characterizes key innovations?
Second, there is often a disparity in time between the
causal origin of an innovation and the ultimate ecological and evolutionary
effect of an innovation. The causes of
evolutionary innovations must be clearly separated from their possible effects
on diversification, niche exploitation, or adaptive radiation (Cracraft,
1990). "Key innovations" that
allow a monophyletic taxon to radiate outwards into a number of new niches can
only be identified post-hoc, after their success has been demonstrated evolutionarily. Immediately after they originate, evolutionary
innovations are just innovations pure and simple. Their prospective future ecological utility as fully elaborated
traits cannot bring them into being initially.
If we wish to understand the actual causal origins of evolutionary
innovations, we must look within the species where the innovation originated,
not at the ultimate macroevolutionary consequences of the innovation. Liem has stressed this point, observing that
"An evolutionary novelty may remain in a stasis for extended times when it
does not convey an improvement in the matter/energy transfer" (Liem, 1990,
p. 161), and "historical tests
also show that there is often a great delay between the emergence of a KEI [key
evolutionary innovation] and the onset of the diversification it is assumed to
cause" (Liem, 1990, p. 165), due
to its newfound ecological utility.
Earlier, he also noted that "adaptive radiations will not occur
until after an evolutionary novelty has reached a certain degree of
development" (Liem, 1973, p.
426). Jablonski (1986, 1990) has
also observed that many innovations fail to persist, let alone trigger a
diversification indicative of ecological utility. Thus, to account for innovations, we must explain the origin and
elaboration of many integrated morphological and behavioral systems that only
rarely manifest much survival utility.
We seem to need a form of iterative Darwinian selection other than
natural selection for ecologically useful survival traits.
Third, the distribution of innovations in animals and flowering
plants is not random with respect to phenotypic features, but is highly
concentrated in features subject to sexual selection. Traditional theories of innovation through natural selection or
through phenotypic constraints and correlations have trouble accounting for
this distribution, which is seen most clearly when we consider the methods of
biological taxonomy. The most common
features used by taxonomists to distinguish one species from another should
logically be the sorts of features most characteristic of (at least minor)
evolutionary innovations. This is an
almost tautological result of the fact that taxa, including species, are in
some sense made up of their innovations (Weismann, 1917): their innovations are
their critical defining features. The
most commonly used defining features for species appear to be primary and
secondary sexual traits, and behavioral courtship displays, which Mayr (1960)
would have misinterpreted as "species recognition signals". And a great many of these traits, used in
the identification of species of animals and flowering plants and discussed in
speciation research, are just the sort of characteristics most likely to have
arisen by sexual selection through mate choice. Studies of evolutionary innovation that rely on reconstructing
explicit phylogenies often rely on such features. For example, in Cracraft's (1990, pp. 31-35) analysis of evolutionary innovations in the Pionopsitta
genus of South American parrots, every single one of the 30 innovations
discussed was a distinctive plumage color pattern or plumage growth pattern
that could have been elaborated through mate choice, such as "bright
orange-red shoulder patch", "crown bright red in male, not
female", "yellow collar around head", or "crown and back of
neck black". Moreover, it is often
easier in taxonomy to identify the species of a male than of a female animal,
because secondary sexual characters are typically more elaborated in males,
whereas females more often retain camouflaged and ancestral forms (Eberhard,
1985).
So, in Eldredge's (1989) terminology, reproductive rather
than economic traits are often used to distinguish between species. In section 7.1, we claim that speciation can
result from a stochastic divergence of mate choice criteria in a sympatric
population leading to a disruption of the mate recognition system within a
given species. If so, most traits
distinguishing one species from another that is, most minor evolutionary
innovations are sexual characters or courtship displays that arose through
mate choice. Moreover, the biological
species concept, which views species as reproductively isolated populations,
virtually demands that the innovations that distinguish one species from
another must function as reproductive isolators that is, as traits subject to
selective or assortative mate choice.
Thus, both the empirical methods of taxonomists and the theoretical
presuppositions of the biological species concept, suggest that most
evolutionary innovations in animals and flowering plants arose through sexual
selection acting on traits capable of creating reproductive isolation between
populations, particularly primary and secondary sexual traits, and courtship
behaviors.
To explain evolutionary innovations then, we need to account
for the following facts. (1) Most
innovations are too complex and well-integrated to have resulted simply from
random mutation or genetic drift, and are too structurally and functionally
novel (i.e. functionally non-neutral)
to have resulted simply from neutral drift.
(2) Many innovations require escape from an evolutionary local optimum,
which natural-selective hill-climbing tends to oppose. (3) Most innovations (i.e. most traits taxonomically useful in
distinguishing species) show very little ecological utility and do not result
in adaptive radiations. (4) Those
innovations that do eventually show ecological utility often show a long delay
between their origin and their proliferation.
(5) Finally, most innovations in animals and flowering plants are
heavily concentrated in phenotypic traits subject to mate choice, and this
distribution cannot be explained by models of innovation through general
phenotypic correlations and constraints.
In general then, the origins of evolutionary innovations must be
explained in terms of some kind of selection between individuals that has
little effect on ecological success and that only rarely leads to
macroevolutionary success.
"Irrespective of whether innovations are perceived as `large' or
`small', they all must arise and become established at the level of individuals
and populations, not higher taxa" (Cracraft, 1990, p. 28).
Thus, innovations that characterize an entire population or species must
be explained at some level above that of simple mutation or developmental
constraints, but below that of macroevolutionary `sifting' between species
(Vrba & Gould, 1986), and aside from that of natural selection for
ecological utility.
The role
of mate choice in generating evolutionary innovations
Sexual selection through mate choice can account for all of
these features of evolutionary innovation in animals and flowering plants. Thus, Darwin's "prodigal variety",
may arise from a long-overlooked wellspring of innovation the effects and
side-effects of mate choice. These
sexually-selected varietal novelties could be called "courtship
innovations." From these humble origins, a few incipient courtship
innovations may continue to be elaborated into more and more complex
morphological and behavioral characteristics.
At various points in this evolutionary course of elaboration, a tiny
minority of courtship innovations and their phenotypic by-products will happen
to show some ecological utility, and may be modified to form new "economic
innovations" that have some ecological utility. And a tiny minority of these economic innovations will prove
important enough that they allow adaptive radiations and later come to be
recognized as "key innovations." Thus, the causal origins of key
innovations may often be the same as the causal origins of courtship
innovations: elaboration of a trait by sexual selection through mate
choice. The net result of sexual
selection's innovativeness may be that sexual selection is to macroevolution
what genetic mutation is to microevolution: the prime source of potentially
adaptive heritable variation, at both the individual and species levels
What kinds
of evolutionary innovations can be generated through sexual selection?
Our theory that many evolutionary innovations arise at first
through the effects of selective mate choice, or as side-effects of
sexually-selected traits, must be clarified and given some caveats. First, and most obviously, the theory
applies only to biological systems where mate choice operates in some
fashion. We have lumped together
flowering plants and animals because they both undergo a form of sexual
selection by animals with nervous systems, either heterospecific pollinators or
conspecifics. Evolutionary innovations
in asexual lineages, and in sexually reproducing organisms that are too simple
to exercise heritable patterns of nonrandom mate choice, must be explained in
some other way. But since innovations
seem to emerge much more slowly and sparsely in lineages without mate choice,
there is less that needs explaining. Thus,
we would expect the frequency distribution of evolutionary innovations to be
highly skewed across lineages, clustered in species subject to high levels of
selective mate choice. As sections 6.1
and 7.2 argue, this is just what we see.
Second, selective mate choice can directly affect only those
phenotypic traits that are perceivable to the animal doing the selecting, given
its sensory and perceptual capabilities.
Thus, mate choice typically applies to macroscopic morphology and
manifest behavior. But it also applies
indirectly to any microscopic morphology, physiology, neural circuitry, or
biochemistry that affects the appearance of the perceivable traits or
behaviors, e.g. the iridescence of bird
feathers carried by microscopic diffractive structures on feathers, the complex
courtship behavior generated by hidden neural circuits, or the persistent bird
song allowed by an efficient energy metabolism. Furthermore, elaboration of these sexually-selected traits may
often have phenotypic side-effects on many other traits, and ecologically
useful innovations may sometimes emerge from these side-effects. So we would expect the frequency
distribution of evolutionary innovations across phenotypic traits to be highly
skewed, clustered around traits that are directly subject to mate choice (such
as genitals, secondary sexual morphology, and courtship behaviors), and
spreading outwards from these traits to others that are structurally,
behaviorally, or developmentally correlated.
Third, as a corollary of the previous point about phenotypic
side-effects, our theory may have fairly limited application to evolutionary
innovation in the traits of flowering plants, apart from flowers
themselves. Pollinators can directly
select for flower traits such as shape, color, smell, and size, but it is
unclear how easy it would be for floral innovations to become modified into
ecologically useful new kinds of seeds, fruits, or chemical defenses, much less
new kinds of twigs, leaves, or roots.
(On the other hand, the evolution of insectivorous plants such as the
Venus Fly-Trap was probably facilitated by the ease with which attractive
flowers can be modified from pollination to predation functions.) Moreover,
despite the fact that the complexity of plant behavior has often been
underestimated (see Darwin, 1876; Simon, 1992), plants cannot use shifts in
behavior and habit to smooth the way for changes of morphological function as
easily as animals do (Darwin, 1883; Bateson, 1988). As a result, the modification of courtship innovations into
economic innovations in plants may be more difficult than in animals. However, polymorphism and sympatric
speciation could almost certainly be facilitated through flower selection by
pollinators, as the data from Eriksson and Bremer (1992) suggest. So the effects of pollinator choice might at
least explain the higher speciation rates and high rates of floral innovation
in flowering plants.