Download Sexual-Selection Models for Exaggerated Traits

AMER. ZOOL., 38:59-69 (1998)
Sexual-Selection Models for Exaggerated Traits are Useful but
Constraining1
GEORGE W.
BARLOW 2
Department of Integrative Biology and Museum of Vertebrate Zoology, University of California,
Berkeley, California 94720-3140
SYNOPSIS. Science is driven by productive hypotheses and technology, but these
may sometimes limit the questions posed. For instance, Fisherian runaway sexual
selection and related hypotheses have helped us understand the evolution of exaggerated visual sexual dimorphism. Species with indistinguishable sexes, however,
may use different behavioral mechanisms when pairing and thus possess different
adaptations. In the monomorphic Midas cichlid (Amphilophus citrinellum), females
chose large aggressive males in a restrained situation, as sexual selection predicts,
but males did not choose. The nuchal hump of males swells coincidently with pair
formation. However, overly large humps were shunned by females while the normal-size hump facilitated sex recognition. This species is polychromatic, and pairs
mate assortatively by color in Nicaragua. Some have suggested the Midas cichlid
might therefore show how sexual selection produces explosive speciation of cichlids
in Africa. All females, however, are biased toward normal-color males. The color
of gold morphs modulates aggressive responses of the other fish. All else equal, the
benefit to gold in a fight equals 15% more weight than the opponent. Pair formation succeeds best when the typically smaller female of a pair is relatively more
aggressive than the male. The pair combination, gold male with normal female, is
difficult to produce; making the female the same size as the male removes the
disability. Pair formation is a negotiated process in which the male tests the aggressiveness of the female relative to self. That puts the behavioral mechanisms of
the male and female in conflict.
way we think about research problems,
where
theory provides metaphorical
An apparatus, tool or technique that
opens new doors to biological questions is "tools." Productive theories, such as that
seductive. Witness the impact of the light underlying runaway sexual selection, need
and then of the electron microscope, or now not but can wind up narrowly posing only
of PCR. Such technology tempts scientists those questions falling within the theory's
to frame only questions that can be an- envelope. Further, its seductive ideas can
swered using the technology, instead of de- inspire near evangelical zeal and thereby
veloping new methods to answer problems deter other approaches.
At the peak of excitement about the
generated from theory or from contrary empirical findings. In animal behavior, tech- adaptationist program, one statement attribnology has had less dramatic impact; two uted to J. B. S. Haldane summed up the
tools, however, are the audiospectrogram attitude. He said, in essence, it matters not
{e.g., Marler and Isaac, 1960), and televi- how the match is lit so long as it is lit.
sion animation {e.g., Clark and Uetz, 1990; Evolution can proceed along different paths
to reach the same solution. Some followers
Macedonia and Stamps, 1994).
The allure of new "tools" extends to the seemed to take the statement to mean discovering how the match is lit is of no consequence to evolutionary questions. Hal1
From the Symposium Animal Behavior: Integra- dane's own research indicates the contrary
tion of Ultimate and Proximate Causation presented at (Spurway and Haldane, 1953).
the Annual Meeting of the Society for Integrative and
I hope to demonstrate the utility of atComparative Biology, 26-30 December 1996, at Altending to how mechanisms, denned as bebuquerque, New Mexico.
2
E-mail: [email protected]
havior and morphology, provide insights
INTRODUCTION
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GEORGE W. BARLOW
into mating behavior in a monogamous
cichlid fish and thereby raise questions
about adaptive significance. The central
theme is the following: Extreme sexual dimorphism stimulated the theory of Fisherian sexual selection. Specific hypotheses
about sexual selection concentrated on exaggerated sexual differences in species that
come together only briefly to mate. Behavioral tasks such as recognition of species
and sex are usually assumed rather than analyzed.
That focus has detracted from our investigation of species with long-term bonding
in which initial attractiveness does enter in
but is only part of the story. The processes
enabling sustained, peaceful relationships
may not be revealed in the standard choice
experiment. The study of these mechanisms
offers a rich opportunity for understanding
both proximate and ultimate mechanisms of
behavior.
I concentrate on the Midas cichlid, Amphilophus citrinellum, an abundant fish in
the lakes and rivers of Nicaragua, whose
sexes are indistinguishable. Most of the
coverage will be on how males and females
in this pair-bonding species form pairs.
How might inter-sexual selection enter the
picture, and how do the fish recognize species and sex? Does early experience with
the care-taking parents play a role? And
what are the consequences of the striking
color polymorphism for mating? Does mating in this polychromatic fish provide a reasonable example of how mate choice could
account for the radiations of African cichlids? The first example illustrates straightforward sexual selection for size and aggressiveness in the male Midas cichlid.
FEMALE CHOICE FOR QUALITY OF MALE
Consistent with sexual-selection theory,
females of the related, modestly dimorphic
convict cichlid 'Cichlasoma' nigrofasciatum, prefer large males (Noonan, 1983;
Keenleyside, 1985). Although the two sexes
of the Midas cichlids are so similar that
most of the time they are indistinguishable,
males in nature (Barlow, 1976) and in the
lab reach a larger size than do females (see
Francis and Barlow, 1993, for an explanation). Further, the male of a freely formed
pair is always appreciably larger than the
female (Barlow, 1976; McKaye, 1986).
Theory predicts a female cichlid prefers
a large and also more aggressive male.
Such males should be superior in obtaining
and holding a territory, and in defending
offspring against predators. However, a
ceiling to this choice behavior is provided
by the male: A large male is less likely to
invest in defending a small female and her
offspring (Coleman, 1993).
Males in the Midas cichlid invest parentally about as much as females (Rogers and
Barlow, 1991). So, a male should be just as
choosy as a female (Trivers, 1972; Burley,
1981). He should prefer a large female because she provides more eggs, and an aggressive female because she can better defend the territory and offspring.
In aquaria, female subjects were offered
four normal-colored treatment males,
viewed through one-way mirrors. When
only size of male was varied, females chose
the largest one. When males differed solely
in aggressiveness, females selected the most
aggressive one (Rogers and Barlow, 1991).
To test whether those results had any
meaning in a semi-natural situation, pairs
were tested in a pond (Rogers and Barlow,
1991). The pairs were first formed in separate enclosures, so mate choice was not an
issue. The testing was simplified by the
fish: Males carry the bulk of territorial defense, and when pairs of cichlids fight pairs,
each sex engages the same sex of the other
pair (Barlow, 1991). As predicted, larger
males were better at holding a breeding territory. The more aggressive males were the
most active in defending their offspring.
Thus, it pays a female to pick a large, aggressive male.
This outcome is consistent with conventional views of the benefits of sexual selection and helps explain selection for larger,
more aggressive males. Male size and aggressiveness can be viewed as exaggerated
traits resulting from sexual selection.
Males, in contrast, did not choose among
the females. As will be explained further
on, the reason for this was that intersexual
interaction was precluded. Some results
now follow that are contrary to predictions
made by models of sexual selection.
UTILITY OF SEXUAL SELECTION
WHAT IS THE NUCHAL HUMP FOR?
Males of many kinds of bony fishes have
a prominent nuchal hump on top of the
head (Barlow and Siri, 1997). The function
of this conspicuous dimorphism, oddly, has
never been experimentally investigated, and
its role has received scant attention.
Males of the Midas cichlid acquire a nuchal hump, but it is prominent only during
pair formation. After that, the swelling recedes. The hump remains in a reduced state
through the long period of care of freeswimming young (Bleick, 1975; Barlow,
1976). Why does the male change his appearance this way?
My favored starting hypothesis was stimulated by the theoretical spirit of the times:
The hump of the male is an exaggerated
trait that has been either intra- or intersexually selected. Several hypotheses are available for intersexual selection of exaggerated
traits, such as runaway selection (Fisher,
1930), sensory bias or exploitation (Ryan,
1990; Basolo and Endler, 1995), an indicator to the female that the male has stored
fat in preparation for parental duties (Searcy, 1982; Burley, 1985), higher resistance
to parasites (Hamilton and Zuk, 1982), and
advertises good genes (Kodric-Brown and
Brown, 1984), perhaps because of hydrodynamic drag (Zahavi, 1975). All predict
that the larger the hump, the more the female should prefer that male.
We considered and rejected other hypotheses, such as antipredation, improved hydrodynamics, and a bumper in fights (Barlow and Siri, 1997). We excluded fat storage because fat content falls during swelling (Bleick, 1975). We ruled out species
recognition because co-occurring related
cichlids express the hump in much the same
way. That left two plausible hypotheses, sex
recognition and quality of male.
In nature, males ready to breed express a
modest nuchal hump (illustrated in Barlow
and Siri, 1997) but females never do. In
captivity, however, where the fish are well
fed and little exercised, some males develop
persistent humps that are vastly larger than
any ever seen in the wild. Some related
cichlids in Central America have huge persistent humps (Meek, 1904). Thus we as-
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sumed selection could produce and maintain such a colossal hump if it offered a
selective advantage.
We therefore proffered four lifelike dummy Midas cichlids with humps that we
called none, medium (the normal modestly
enlarged hump), large and huge. If females
responded progressively more to ever larger
humps, that would indicate intersexual selection but would not rule out sex recognition. If, however, females responded most
to the dummy with the normal size of
hump, that would be evidence for sex recognition, and would rule out sexual selection.
Females responded significantly the most
to dummies with the normal hump, supporting sex recognition but rejecting sexual
selection. Males did not differ significantly
in their responses to the dummies, though
they reacted most to the dummy with no
hump; that response profile is also consistent with sex recognition because lack of a
hump bespeaks a female.
Sexual selection was a useful starting hypothesis, and in its broadest meaning (Andersson, 1994) could apply here. However,
as Andersson defined sexual selection, it is
virtually synonymous with mate choice and
becomes an umbrella covering species and
sex recognition. As such, the term loses
utility. It also detracts from sorting out the
underlying behavioral mechanisms.
MATE CHOICE IN RELATION TO COLOR
The Midas cichlid originally attracted attention because it is strikingly polychromatic in many of the lakes in Nicaragua.
About 8% of the adults of both sexes are
gold because they have lost their melanophores at various ages, revealing the underlying xanthophores (Barlow, 1976; Dickman et al, 1988). We call the prevailing
gray morph normal. A convincing explanation for the apparently stable polychromatism has not emerged (but see Dickman
et al, 1990).
Polychromatism and color-assortative
mating in the Midas cichlid have inspired
conjecture about sympatric speciation
(McKaye, 1980; McKaye and Stauffer,
1986; Meyer, 1990). Assortative mating
was reported in a seminatural pond (Bar-
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GEORGE W. BARLOW
low, 1976) and in a lake in Nicaragua
(McKaye and Barlow, 1976). In the lake,
separation by color was more complete;
about 95% of pair members were the same
color. A reasonable conclusion is the different colored morphs choose one another
as mates. Thus, discovery of a behavioral
mechanism in mate choice shaped thinking
about the Midas cichlid as a model for speciation in the African Great Lakes. However, how that assortative mating arises was
not known.
We therefore asked whether a Midas
cichlid would choose its own color morph
for a mate when given an unfettered choice.
Early experience with parents or siblings
has been implicated in mate choice by cichlids (Greenberg, 1963; Siepen and Crapon
de Caprona, 1986); that could accelerate
speciation, if other conditions are met
(Maynard Smith, 1966).
The first test of "sexual imprinting"
(Barlow and Rogers, 1978) was ambiguous
and less rigorous than the second (Barlow
et al., 1990). The second addressed whether
color of parents, siblings or self influenced
choice of mate. Each female subject was
repeatedly offered a choice of a new gold
and new normal male. The treatment males
were presented behind a one-way mirror,
precluding interactions. As before, male
subjects did not respond when prevented
from interacting with the female.
The choices of the females were muted
by their tendency to visit back and forth
between the males, and so choice was detected only statistically. Females were not
influenced by their own color. The colors of
their parents and siblings had a slight effect.
The clearest difference was a significant
bias among females from all rearing conditions for males having the normal color
pattern. Weber (1976) reached the same
conclusion with the related convict cichlid,
' C nigrofasciatum.
That outcome indicated female Midas
cichlids have an inherent bias for the normal color pattern. Some other forces must
consequently be working to produce assortative mating. Vacillating by the females
suggested that color differences are not of
primary importance and that they are
weighed against other aspects of the males,
such as aggressiveness. The males, who
were matched for size, could view other
males out of the females' line of vision, and
they interacted with them. Variation in that
interaction probably influenced female
choice (see below).
EFFECT OF GOLD COLOR ON AGGRESSION
Aggressiveness of the fish has a central
role in pair compatibility. So it is important
to understand how aggression is modulated.
Gold coloration profoundly affects the fish
that perceives it (see also Evans and Norris,
1996). The response depends on the context, however (McKaye and Barlow, 1976;
Barlow and Francis, 1988; Barlow and Siri,
1994): When a dominant fish responds to a
gold subordinate, in comparison with a normal-colored one, then the dominant fish increases attacking. But if the subject is itself
subordinate, or uncertain, then a gold opponent depresses aggressiveness.
The probability of winning also varies
with the size of the contestants. When the
normal morph is 15% heavier than the gold
one the probability of either winning is 50%
(Barlow, 1983). Hence being gold confers
an advantage equivalent to being 15%
heavier than the normal opponent, all else
equal. With both contestants the same color,
a weight difference as small as 2% can tip
the outcome toward the heavier fish (Barlow et al., 1986) so a 15% difference is
consequential.
Other experiments proved that golds and
normals are equally aggressive (Barlow and
Wallach, 1976; Barlow and Siri, 1994). The
effect is thus not genetically linked to coloration but is instead a property of the perception of gold. I stress this because the
point is regularly misunderstood to mean
that golds are the more aggressive morph.
PAIR FORMATION AS AN INTERACTION
The long prevailing perception of pair
formation in monogamous cichlids had the
male establishing a breeding territory where
the female approached him (Baerends and
Baerends-van Roon, 1950). However, evidence is accumulating suggesting pair formation may precede or be coincident with
setting up a territory (McKaye, 1977; Barlow, 1991).
UTILITY OF SEXUAL SELECTION
In the field, pairs of Midas cichlids apparently form within loose aggregations.
Then they move into the breeding area
where they cooperate in obtaining a territory. Observing the moment of pair formation in nature, however, is difficult. In a
large artificial pool, females competed for
males within heterosexual groups in a way
previously unseen in confined aquaria (unpublished data, G.W.B.). A crucial step is
when some female swims head on at the
dominant male while expanding her opercles, normally a threat gesture. The male
mirrors her behavior, as though testing her
resolve. At the last moment, she veers off
and the two fish brush one another in passing, a behavior pattern called slipping. Females compete with one another, one proposes to the male, and the male accepts or
rejects her. This is central to understanding
assessment and pairing in this species.
All but one of the studies to this point
had prevented behavioral interaction between the subjects and the treatment fish.
The experiments were purposely so designed despite believing interaction is paramount. That was done because of fear the
responses of the treatment fish to the subject would override the effect of the variable being manipulated, such as size or color. The next experiment employed a situation that not only permitted interaction but
depended on it.
The immediate objective was to probe alternative predictions about the role of interaction in pair formation. In the process
of forming a pair, many of the modal action
patterns used are the same as those in a
fight. The focus was therefore on determining the difference in aggressiveness between a male and a female that favored successful pair formation. The plan of the experiment was generated by three hypotheses
(Barlow, 1992).
The first, called parity, hypothesized that
male aggression is a balance between selection for defending the territory and selection against being too aggressive to mate
with the female. It predicted an optimal difference in aggressiveness with the male being the more aggressive mate.
The second hypothesis was complementarity: To minimize intrapair fighting, some
63
ideal sum of the male's and female's aggressiveness is optimal.
The third hypothesis was female choice
for the most aggressive male. This is a direct application of the sexual-selection
model, such as proposed by Noonan (1983)
for ' C nigrofasciatium.
The results (Barlow, 1992) falsified all
three hypotheses. The exercise, however,
revealed the role of relative aggressiveness
in pairing. It also demonstrated a conflict in
behavioral mechanisms that runs contrary
to simplistic views of mate choice.
Normal females were the test subjects.
They were given a choice of two appropriately larger normal males of about the same
size. We wanted to determine female choice
first when restrained by a barrier and then
ask whether the same female could successfully mate with the unrestrained male
of her choice.
On the first day, the female could visit
both of two males. The males were held
back by a large-mesh screen that permitted
exchange of visual, chemical, possibly
acoustic, and hydrodynamic stimuli and
slight physical contact. On the second day,
the screen was removed. Being smaller than
the males, the female could pass through
slits adjusted to her size but the larger males
could not.
One crucial detail: The aggressiveness of
all three fish was quantified in the test arena
on the day before the observations by presenting a mirror to each fish.
Female choice was refreshingly crisp.
She spent all or nearly all her time with
only one male instead of visiting back and
forth as in earlier experiments. However,
even here simple extrapolation to the natural, unrestrained situation can be misleading.
When the barrier was taken away, 43%
of the females either did not or could not
pair with the male of choice. The usual
cause of failure was excessive attacking by
the male. Of the rejected females, 29%
switched to and paired with the male they
had previously neglected. Clearly, female
choice was overridden by male rejection.
But why did those pairings fail?
To test the parity hypothesis, I had plotted the sum of male and female courtship
64
GEORGE W. BARLOW
as a function of the difference in aggression
scores for each pair. When the barrier was
in place, no relationship emerged. Although
the male and female seemed to interact
through the barrier, in actuality they behaved semi-independently. Each was to a
degree insensitive to the actions and responses of the other. For instance, some
males repeatedly dashed at the screen and
bit it in an attempt to attack the female. The
females continued to court instead of withdrawing.
When the barrier was removed, a clear
pattern of behavioral interaction emerged in
the successful pairs: The more the previously measured aggression score of the female exceeded that of the male, the larger
became the sum of their combined courtship acts, and conversely the smaller the
sum of aggressive behavior. Pairing success, as measured by total courtship, was
not just a matter of more aggressive females, nor of just less aggressive males.
The relative score was the powerful predictor.
Even though the differences in relative
size were small, the unintended variation in
size also influenced pairing. Increasing female size equated to increasing aggressiveness. The larger the female relative to the
male, the more the pair courted.
The experiment demonstrated the primacy of relative aggressiveness between
the male and the female. It also showed that
aggressiveness and size can be traded off.
Gold color is tantamount to size or aggressiveness, gold should also have a profound
effect on mating.
EFFECT OF COLOR ON MATING SUCCESS
Although the following comes from an
early experiment, it makes more sense now
in light of female bias for normal color and
the effect on pairing of relative size and aggression. In his doctoral research here, David Noakes noticed that producing compatible pairs of gold males and normal females
was difficult. That led to the following experiments (Barlow et ah, 1977).
We used all four combinations of color
and sex, and the female of each pairing
weighed 15% less than the male, a typical
size difference in nature. First, we recorded
time needed for a female to spawn when a
screen separated her from a male. All pair
combinations spawned on average in 14
days. Restraining the fish prevented differences from emerging.
The experiment was repeated, but now
the screen was opened. Those pairs with
normal females failed quicker (mean two
days) than those with gold females (mean
six days). We concluded that gold color inhibits male aggressiveness.
About half of the pairs failed in all colorcombinations except for one: Gold male
crossed with normal female stood out from
the others because only 14% of the pairs
were successful.
Pair formation in this and many other
species of pair-bonding cichlids looks at
first like a ritualized fight. We reasoned that
the smaller size of the normal female, compounded by the imposing color of the gold
male, made her too timid. Recall that gold
color in a contest confers an advantage
worth 15% by weight.
We predicted that if gold males were
paired with normal females equal in size,
her increase in size would compensate for
his color advantage. That was the case.
Mating success climbed to about 60%, the
same as, or better than, the other color combinations with small females. Thus, the results accord with those on the role of relative aggressiveness in promoting pair formation.
DISCUSSION
The nuchal hump as a sexually selected
trait
Understandably, and following Darwin
(1871), theory underlying sexual selection
has focused predominantly on exaggerated
sexual dimorphism. The well-known models include Fisher's (1930) runaway-selection, sensory bias or exploitation (Ryan,
1990; Basolo and Endler, 1995), physical
fitness for parentally care-taking (Burley,
1985; Hoelzer, 1989), and good genes in
general (Kodric-Brown and Brown, 1984);
resistance to disease (Hamilton and Zuk,
1982) and the handicap principle (Zahavi,
1975). All of these attempt to account for
exaggerated traits and therefore necessarily
UTILITY OF SEXUAL SELECTION
rest on a supernormal type of behavioral
mechanism (Tinbergen, 1951; Baerends and
Kruijt, 1973) in which bigger or more ornamented is better.
The example of the nuchal hump in the
Midas cichlid, however, demonstrated that
bigger is not necessarily better (Barlow and
Siri, 1997). Females responded most to an
intermediate size of hump, and one that corresponded to the size typically seen on
males in nature. The males, in contrast, reacted most to dummies with no hump; lack
of a hump signifies female. Selecting the
correct sex does play a role in one's fitness.
By that criterion, choice based on the presence or absence of the nuchal hump could
be considered sexual selection. So classifying it, however, detracts from more specific behavioral adaptations such as sex and
species recognition.
Mate choice and sexual conflict
The focus on exaggerated traits was initially productive. With some exceptions
(Burley, 1977), workers concentrated their
efforts on species that are highly dimorphic,
typically polygynous, and meet only briefly
for fertilization. Those dimorphic species,
however, may prove an example of a biological "tool" that detracts from the pursuit
of other aspects of mating behavior.
A monomorphic species, such as the Midas cichlid, presents a different challenge
and possibly different answers. I consider it
monomorphic because the sexes are visually indistinguishable even though in pairs
the female is invariably smaller than the
male. I do this because the male and female
look alike and their size distributions overlap as adults. Burley (1981) categorized a
species as indistinguishable if the individuals reveal a morphological clue to their sex
only at certain times. Many such monomorphic species exist in diverse taxa. Judging from our experiments, if they have prolonged pairing, mating is more than initial
preference.
In one respect, only, pairing in the Midas
cichlid fits the scenario for exaggerated
traits. Given a choice, females prefer the
larger and more aggressive male (Rogers
and Barlow, 1991). The problem is that her
preference can conflict with and be coun-
65
tered by that of the male. Males reject females that are not aggressive enough in relation to the male's aggressiveness (Barlow,
1992). Therefore, mate choice in this pairbonding species with similar-appearing sexes, is a negotiated relationship between
male and female; it is not a simple matter
of choice as is so typical for polygynous
species {e.g., Weatherhead, 1990).
These findings give us pause and compel
one to think about the possible adaptiveness
of such a mating arrangement. Why males
of a biparental species should prefer more
aggressive and large, hence fecund, females
is easy to understand, as is female preference for large, aggressive males. But that
puts the two sexes in conflict. Females may
not be able to form pairs with such males.
Does that mean in nature successful males
are the less aggressive ones? How would
that work?
The negotiated nature of pairing was also
demonstrated in the experiments on mate
choice (Barlow et al., 1990) as contrasted
with forced pairings (Barlow et al., 1977).
Female choice of male by color morph,
when made through a one-way mirror, was
for the normal color. We (Barlow et al.,
1990) concluded that her choice was driven
by innate recognition of the primitive color
pattern. But when males and females were
placed together pair-wise, only about 50%
of the pairs could successfully form, and
that included normal male with gold female. One combination, gold male with
normal female, had a success rate of about
one-third of that.
Thus one behavioral mechanism, the inherent preference for normal color, is overridden by other behavioral mechanisms.
Gold color, because of its effect on the aggressiveness of the other fish, profoundly
influences the likelihood of forming a functioning pair. Unfortunately, we still do not
understand why, in nature, most fish pair
assortatively by color. The answer must lie
in some combination of behavioral mechanisms. One of the most prominent of these
is probably the effect of gold on the process
of negotiating a "peace treaty."
Mate choice and speciation in cichlids
The complexity of pair formation in pairbonding cichlids should be a caveat to using
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GEORGE W. BARLOW
assortative mating in the Midas cichlid as a
model for speciation among the brieflypairing African cichlids. Evolutionary biologists have sought a plausible mechanism
for the spectacular radiation there of cichlids into hundreds of species, many of them
polychromatic. The most frequently proposed mechanism is sexual-selection (Kosswig, 1947; Dominey, 1984; Mayr, 1984). In
this scenario, some females prefer to mate
with one color morph and other females
prefer the other color; that is the "foot in
the door" that leads to a separation of one
gene pool into two (see also Seehausen,
1996, recently summarized in Stauffer et
al., 1995).
The relevance of the Midas cichlid to this
situation was noted by McKaye (1980,
1991). He found that pairs of gold morphs
breed in relatively deep water while the predominant normal gray morphs breed in
shallow water. Based on assortative mating
and differential depth distribution, he suggested the two morphs were potentially two
species.
Meyer (1990) discovered that the pharyngeal jaw apparatus (PJA) of the Midas
cichlids is also polymorphic and might
present an avenue for sympatric speciation.
Liem (1973) had argued the PJA of cichlids
is an innovation that facilitated the radiation
of the African species. The polychromatism
of the Midas cichlid correlated with diet
and depth distribution. Unclear, however,
was whether the difference is genetic or
phenotypic (Meyer, 1990); Axel Meyer has
now confirmed that the morphs do not differ genetically (personal communication).
Meyer further suggested color of morph
and type of PJA covary. The differences
were significant, but they applied only to
one lake during one season. From the conjunction of depth distribution of snails and
breeding, PJA type and assortative mating
by color, and following Maynard Smith
(1966), Meyer guardedly suggested this situation might be an instance of sympatric
speciation in the making, and with unspecified relevance to radiations in the African
Great Lakes. Later workers on the African
cichlids {e.g., Greenwood, 1991), have cited the papers of McKaye (1980) and Meyer
(1990) as providing a possible model for
understanding speciation through female
preference of male color.
The Midas cichlid, however, is inappropriate for the situation in Africa. It and allied species (Barlow and Munsey, 1976)
may be undergoing a modest radiation in
Nicaraguan lakes (Stauffer et al., 1995; personal communication, E. van den Berghe),
but color differences are slight, such as a
more yellowish cast to one putative species.
The three described sibling species are all
colored alike, and one of them, Amphilophus labiatum, is polychromatic in much
the same way as is the Midas cichlid (Barlow and Munsey, 1976). Likewise, most of
the undescribed species are polychromatic.
If assortative mating by color were the
key to sympatric speciation in Nicaragua,
then the different species should have been
all gold or all normal. We should find sibling species, some of which are all-gold and
some of which are all normal. That the different and apparently recently evolved species are all much the same color is also contrary to the proposition that color differences have lead to their speciation (see Seehausen, 1996). Rather, because most of the
other cichlids in Central America are differently colored (Barlow, 1974), color differences appear to reinforce speciation rather than produce it.
Why doesn 't the polychromatic Midas
cichlid speciatel
The key issue in the Midas cichlid, however, is assortative mating. What prevents
them from evolving into two species? The
reason appears to lie in the timing of the
loss of melanophores, the change in color
from normal to gold. Within a cohort from
a single pair, color change commonly occurs first in juveniles that are about six
months old, but some adults may still be
normal in color when two or more years
old. Some first-generation offspring of
wild-caught fish did not change color until
they were five years old. Yet they breed first
when about 18 months old. K. R. McKaye
(personal communication) has recently seen
juveniles in Lake Xiloa that have metamorphosed when about one month old, but the
situation there has been disturbed by humans.
67
UTILITY OF SEXUAL SELECTION
Commonly, a fish could, therefore, mate
and reproduce first as a normal morph then
later as a gold one. That would break down
the separation into genetically different
groups even in the presence of assortative
mating.
One way to keep the gene pools separate
would be for the fish to imprint on the color
of their parents. The young are protected by
their parents for about one month, so they
have ample opportunity to learn about the
color of their parents and clearly do (Noakes
and Barlow, 1973). However, for mating,
they do not imprint on their parents' color
(Barlow et al, 1990).
The choice experiment as a possibly
constraining "tool"
The seeming conflict in the findings for
restrained versus unrestrained mating
should give both encouragement and caution to experiments on mate choice when
potential mates are presented behind barriers, or as TV images or dummies. Such experiments are invaluable in teasing out the
behavioral mechanisms, but they need to be
interpreted guardedly, especially when not
gauged against the natural situation.
The role of the concept of sexual selection
The concept of sexual selection has
proved productive in understanding evolution. But now use of the term has broadened
so beyond the Fisherian model that it encompasses nearly all aspects of mating, and
in monogamous as well as polygynous species. Even species recognition is explained
as sexual selection, at least in a solitary species (Ryan and Rand, 1993). Plants manifest sexual selection (Arnold, 1994), and so
do sperm (Willson, 1990).
This perspective has been put forth by a
number of authors (Andersson, 1994) and
is expressed by Wiley and Posten (1996, p.
1372): "Sexual selection is best defined as
a difference in fecundity as a result of heritable differences in access to mates." Although this perspective has stimulated
abundant good research, such an over-arching view can detract from sorting out and
comprehending other aspects of mating behavior.
An understanding of the behavioral
mechanisms of mate choice provokes hypotheses about ultimate explanations. And
ultimate explanations stimulate more focused questions about behavioral mechanisms. To understand the evolution of behavior, both proximate and ultimate explanations are needed.
ACKNOWLEDGMENTS
I am grateful to many people too numerous to mention, unfortunately, who have
contributed to this program in ways large
and small over the years, but they are all
thanked. I am also indebted to Ron Coleman for his careful reading of the manuscript and for stimulating differences with
anonymous referees. The National Science
Foundation, U.S.A., supported the program
over several years, as did the Committee on
Research at the University of California,
Berkeley, for which I say thank you.
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Corresponding Editor: Paul A. Verrell