Download Mimetic butterflies and punctuated equilibria

Biological Journal of the Linnean Society (1983), 20: 277-300. With 9 figures
Mimetic butterflies and punctuated equilibria:
some old light on a new paradigm*
J. R. G. TURNER
Department of Genetics, University of Leeds, Leeds L S 2 9JT
Accepted for publication August 1982
The horns of a dilemma are usually on the same bull-Spanish
A plague 0’both your houses- Veronese imprecation.
proverb.
Although some hypotheses explain the world better than others, making ‘pluralism’ an untenable
position, it is the case that scientists frequently set up as alternative hypotheses, one of which must
be rejected, models which are merely compatible aspects of some other valid hypothesis that
embraces them both. For example, Mullerian mimicry was once supposed to evolve either by a single
large change or by gradual convergence (the assumption of gradualism is such that the second
alternative has usually been regarded as correct). Yet our genetical research with Heliconius
indicates that both processes take place, one after the other, when Mullerian mimicry evolves.
A reconstruction of the most plausible route, through time and space, for the evolution of
mimicry in Heliconius erato and H . rnelpornene is used to suggest that two currently popular
controversies are similarly futile: the allopatric and parapatric models of race formation are
considered to be the extremes of what in nature is a continuum of populations showing varying
degrees of partial isolation (ecological change rather than stoppage of gene flow being the driving
force in race formation); and it is shown that jerky evolution of the type now interpreted as evidence
for ‘punctuated equilibria’ and ‘hopeful monsters’ can be produced by changes in the frequencies of
major but ordinary gene mutations in response to changing ecological conditions, a phenomenon
well accounted for in neo-Darwinian theory.
KEY WORDS:-Jerks
- Heliconius -
refuges - mimicry
-
cladistics.
CONTENTS
Of adversaries and inquisitors . . . . . . . . . . . . .
Gradual or sudden evolution? A dynamic theory for Mullerian mimicry . . .
An old battle . . . . . . . . . . . . . . . .
Gradual convergence and persistent rings . . . . . . . . .
The two-stage theory . . . . . . . . . . . . . .
Allopatric or parapatric race formation? A geographical reconstruction of the recent
The ice ages in the Amazon . . . . . . . . . . . .
Disorderly extinction on islands . . . . . . . . . . .
Gradualism or punctuation? A phyletic reconstruction . . . . . . .
Switching niches . . . . . . . . . . . . . . .
Estimating the ancestors . . . . . . . . . . . . .
Evolutionary trees.
. . . . . . . . . . . . . .
Evolution by jerks.
. . . . . . . . . . . . . .
Evolution: an old and general theory . . . . . . . . . . .
References. . . . . . . . . . . . . . . . . .
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278
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28 1
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285
286
289
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290
29 1
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295
298
*This paper was originally presented at the International Symposium on Biogeography ‘Time and Space in
the Emergence of the Biosphere’ held to celebrate the centenary of the British Museum (Natural History),
6-10 April 1981, under the title ‘Mimetic butterflies and Amazorian refuges; a model for adaptive radiation in
the tropics’. See also Sims, Price & Whalley (1984).
0024-4066/83/070277
+ 24 $03.00/0
277
0 1983 The Linnean Society of London
278
J. R. G. TURNER
OF ADVERSARIES AND INQUISITORS
The inquisitorial system ofjustice is based on the idea that the best way to
arrive at the truth about things is to build up an extensive and self-consistent
picture of all the relevant events. I shall use something like this system here to
try to reconstruct the evolution of some remarkable mimetic butterflies in the
South American genus Heliconius.
T o make such a comprehensive reconstruction we need to know the
evolutionary forces acting on the populations, the genetical outcome of these
forces, the historical theatre in which these events were played out, and the
genealogy of the populations. Thanks to two decades of research, we now have
this information for Heliconius; the only comparable case-history is of the
Hawaiian Drosophilas.
The adversary system, an alternative to inquisition, used in ‘English’ courts,
in which the two ‘sides’ in a dispute try to prove their correctness by producing
the crucial evidence that will demolish the other’s case, is not best suited to such
things as discussing the artistic merit of books and pictures, nor to arranging
divorce settlements with a minimum of bitterness. The adversary system in
science, in which we are invited to reject one hypothesis in favour of another, sits
uncomfortably in those disciplines in biology and the earth sciences where
history is an important element. Even when no unverifiable historical statements
are involved, adversary arguments in science often end only with the
appearance of a system of explanation that fuses elements from both sides: what
disputant in the eighteenth century could have imagined that development was
neither epigenetic nor preformed, but encoded in a digital program?
In the course of reconstructing our case history, I shall look at three instances
of opposing hypotheses, and ask how sensible it would be to declare the case in
favour ofone or the other. O u r full genetical findings are being published elsewhere
(Sheppard et al. in press); for other reviews, see Brown (197713, 1979, 1981) and
Turner (1976, 1977a, 1981, 1982); as extensive bibliographies are given by
Brown (1981) and Turner (197713, 1981), I have not attempted to give
comprehensive citations.
GRADUAL OR SUDDEN EVOLUTION? A DYNAMIC THEORY FOR MULLERIAN MIMICRY
An old battle
F. A. Dixey and G . A. K. Marshall spent much time and paper belabouring
each other over the evolution of Mullerian mimicry, that is, the mutual,
protective resemblance of two or more distasteful and warningly coloured
species (Dixey 1896, 1907, 1909; Marshall 1908, 1909). The contest, conducted
with perhaps ironical courtesy, must have been entertaining but, like boxing,
ultimately unedifying to the spectators. Each presented his theory with much
skill; neither could demolish the other’s theory; they pummelled each other to a
standstill.
Dixey (1896, 1907), taking many of his examples from the South American
butterflies, had proposed that Mullerian mimicry arose by the mutual
convergence of two butterflies to some pattern halfway between the two,
perhaps taking some features from one species and some from the other.
Marshall (1908) pointed out that only the species which was less protected (by
MIMETIC BUTTERFLIES
279
being less numerous or, as Dixey (1909) later added, less distasteful) would
evolve, by adopting the pattern of the better protected species; the adoption of a
marking from the less protected species would be of no advantage to the better
protected. These models look decidedly like exclusive alternatives, yet the reason
for the stalemate is that both are correct. What was missing at the time was an
understanding of gene action and of animal behaviour.
Gradual convergence and persistent rings
What has to be explained by any model for the evolution of Mullerian
mimicry is not simply that there is some mutual resemblance between
distasteful species. As the cornerstone of Mullerian mimicry is unformity, the
repetition to the predator of a pattern which it has learned to be the mark of
something nasty, there are two paradoxes to be explained. First, there is the
fact, as true for temperate zone bumblebees and Hawaiian wasps as it is for
tropical butterflies, that not all the unpleasant animals that one might
reasonably expect to be Mullerian mimics resemble one another. In Europe
there is some diversity of bumblebee pattern, with the black and yellow striped
patterns being markedly distinct from the red-tailed black bees (Plowright &
Owen, 1980); each island of the Hawaiian group possesses up to four distinct
patterns of wasp (Perkins, 1912); in the neotropical forests the long-winged
distasteful butterflies occur in five rather distinct patterns, or mimicry ‘rings’,
each containing a large number of species (Papageorgis, 1975). How do we
explain the fact that the members of these rings are frequently very similar
indeed, even when they belong to different families, while the rings themselves
remain so distinct?
Imagine a distasteful species, showing some range of phenotypic variation,
which can be represented for simplicity on a linear scale (shaded curve in Fig.
1A). It is known from experiments (reviewed by Turner, 1977c; but see
especially Duncan & Sheppard, 1965; Goodale & Sneddon, 1977) that
predators ‘generalize’, that is to say, tend to avoid patterns which are similar
but not identical to the one they have learnt goes with a nasty experience; this
avoidance, not surprisingly, decreases the more remote is the resemblance. We
can represent this by a ‘curve of protection’ (heavy line in Fig. 1A ) , falling away
on either side of the warning pattern, but protecting to some extent quite a variety
of other patterns. If we now imagine that there are two species, A and B, not
identical but similar enough for the curve of protection generated by one to
overlap the existing range of variation of the other (Fig. lB), then we can see
that, as individuals in A which look rather like B are better protected than those
varying from the norm in the opposite direction (because the former are
protected both by being recognized as A and, sometimes, mistaken for B,
whereas the latter are only recognized as A ) , and similarly for species B, then
both species are subjected to selection for mutual convergence toward some
pattern in between the two of them. Given the appropriate hereditary variation,
they will in time become rather good Mullerian mimics; in this way, any
number of species can be built up into a Mullerian mimicry ring.
It is not difficult to see why several rings persist in the same habitat: if two
species are so dissimilar that predators never mistake one for the other (that is, if
the curves of protection do not overlap the phenotype distributions-Fig.
1 C),
J. R. G. TURNER
280
I
tA
Phenotype
t
Selection
0
X
Selection
b
Y Phenotype
Figure I . A model for the evolution (or non-evolution) of Miillerian mimicry. The horizontal scale
represents a range of potential phenotypes. The phenotypes of existing species, with their normal
variation, are shown by the shaded areas. A. The distastefulness of the species, allied to
generalization by the predators, causes not only the existing patterns to be protected but also
potentially protects a wider range of patterns than actually exists (heavy curves). Selection on the
species is normalizing, tending to keep its phenotype constant. B. Two species which already
resemble one another fairly closely, so that each gains some protection from the existence of the
other, are selected for gradual mutual convergence and will become Miillerian mimics. C. Two
species with markedly different patterns will not converge on one another, as the predators never
confuse them (neither protection curve overlaps the other distribution). Thus two or more warning
patterns may persist indefinitely in the same habitat. D. If two species are not equally protected,
Miillerian mimicry may evolve between them, even though they do not confuse the predators, if the
less protected (Y) can produce a major mutation with a pattern not necessarily perfectly resembling
pattern X but at least lying within the range ab. After Sheppard ct al. (in press).
then there is no selection for them to converge on one another. If, as a Gedankenexjeriment, one were to create a distasteful butterfly fauna with a continuous and
wide range of patterns, this would gradually condense, like planets out of a
cloud of dust and gas, into a number of mimicry rings, very distinct from one
another in pattern, but with a high degree of mimicry within each ring. This is
the situation now found in the neotropical forests.
MIMETIC BUTTERFLIES
28 1
The two-stage theory
Each of these mimicry rings will be subjected to quite strong stabilizing
selection: as is shown by the protection curves, deviant individuals tend not to
be recognized as members of the ring, and predators will sample them on the
off-chance that they are a new and palatable prey, an effect confirmed
experimentally by Benson (1972) who painted out part of the pattern of some
Heliconius erato in Costa Rica; the altered butterflies were recaptured less
frequently, and when recaptured showed more beak-damage, than the controls,
carrying the same weight of paint but with an unaltered pattern. Hence the
second paradox that we have to explain is the geographical variation which is
found within the mimicry rings: once established, a bad brand-image should be
kept, and yet all the mimicry rings of Latin American butterflies vary from one
place to another. The most numerous of them, the ‘tiger’ ring of black and
orange heliconids, ithomiids, danaids, pericopids and others, has black
hindwings in Guiana, orange hindwings on the Amazonas, a white forewing
splodge in southern B r a d , a mahogany colour in Bolivia, a characteristic
striped appearance in Central America and so on (Moulton, 1909). Within each
species (many of which are themselves found through most or all of the range of
the mimicry ring) there has been considerable geographical divergence, in the
face of normalizing selection to maintain the same pattern. Perhaps the most
extreme case is found in the red-and-yellow (or ‘postman’) ring, two members of
which (Heliconius melpomene and Heliconius erato) are shown in Fig. 2. Within each
species, this extraordinary diversity has arisen from some common ancestral
pattern.
Mutations of single genes can produce quite marked alterations in the pattern
of a butterfly (see for instance the catalogue by Robinson, 1971). The chance
that accurate mimicry can arise in this way is remote, but our model shows us
that accurate mimicry is not needed to get evolution started. Consider Fig. l D ,
in which distasteful species X, being more numerous or nastier, is better
protected than species Y. Any mutation of Y which produces a pattern
somewhat-but
not necessarily exactly-like
that of X (in the diagram by
falling within the construction ab) will at an advantage to the original pattern
of Y, and the mutation will increase in frequency under natural selection until
all Y butterflies have the new pattern. Y will therefore undergo one-way
convergence to become a possibly rather poor Mullerian mimic of X.
Paradoxically, although individuals in species X will be better protected once
Y has become a mimic, all the evolutionary work is done by Y. Mutants of
X which happen to resemble Y will be less well protected than the original X
pattern, and X does not, at this stage, converge to Y.
It is an important corollary of this model that convergence of this kind,
involving a comparatively large mutation, will occur only when the gap
between the patterns is not too wide. If several large mutations are required to
produce the mimicry, then the probability of their occurring all at once is very
small, and the butterflies will remain distinct. Brown & Benson (1977) described
a fine example of this in Heliconius hermathena, a species which occurs in scattered
colonies in the Amazon basin (Fig. 3 ) . In most places, it flies with other
Heliconius rather remote from it in pattern (differing, for instance, in the colour
and shape of both the bands on the forewings and the marks on the base of the
282
J. R . G. TURNER
Figure 2. Parallel variation and distribution of the Miillerian mimics Heliconius melpomene (left) and
Heliconius erato (right). Narrow hybrid zones omitted (Turner, 1971). Colours are black, red
(shaded), and yellow, or (in Ecuador) white. From Turner (1975, 1981).
wings); no convergence has taken place. But at one locality where it flies with a
race of Heliconius melpomene which differs from the normal pattern of
H . hermuthenu only in lacking the yellow wing bars, a single mutation removing
most of these marks has become established in H . hermuthenu, making it a quite
satisfactory mimic (Fig. 3 ) .
Thus if a distasteful butterfly flies with another species, not too different in
pattern, but much better protected, it is likely to become a Mullerian mimic of
that better protected species, by the establishment of a mutation of fairly large
effect. This clearly would account for the kind of divergence seen between the
races of Heliconius erato and its co-mimic H . melpomene. But, in addition, once the
new mutation has established itself, the two species are in the position described
in Fig. lB, in which they are selected for gradual mutual convergence. In this
way, both species Y and species X will be altered. The importance of this is that
when a well protected mimicry ring catches a new species by mutation, there
will be some smaller alteration in the pattern of the ring itself. Thus, warningly
MIMETIC BUTTERFLIES
283
Figure 3. Miillerian mimicry evolving only when two species are sufficiently similar for the gap
between them to be bridged by a single mutation. Heliconius hermathena ( 0 )is normally non-mimetic
and flies with forms of H. erato (top right) to which it bears little resemblance. I n a few localities it
flies with forms of H . crato and H . melpomene (shading) which it already resembles except for the
yellow bars. In one of these localities ( O ) ,H. hermathena has become a Miillerian mimic by almost
losing its yellow marks. After Brown & Benson (1977); Sheppard et al. (in press).
coloured species will evolve in two ways: by large changes when they are caught
by a well protected ring, and small ones when they themselves do the catching.
It is postulated, therefore, that in different areas H . melpomene and H . erato
have been caught by different, locally abundant, mimicry rings, or have
themselves been in rings which have caught different species in different places.
We cannot be certain which other species were originally involved: melpomene
and erato are always involved in mimicry with other butterflies, many of them
belonging to familes known to be distasteful, but of course the species which
originally effected the capture at some time in the past may no longer be
abundant, or may even be extinct, or have itself been captured by another
mimicry ring. Likely candidates are various pierine species in Venezuela,
acraeines in Per6, and other Heliconius in the Amazon basin. We are for the
moment rather short of candidates for the yellow-barred races found at various
places all the way from Central America to southern Brasil; perhaps here the
original mimic has become extinct, or was the now rather rare species Heliconius
(eleuatus) besckei, which does have this pattern, or the now allopatric H .
hermathena (see also Fig. 3).
If the above model is correct, then the differences between the races of
Heliconius melpomene (and between those of H . erato) should turn out to be due
partly to genes of quite large effect, and partly to the modifying genes of smaller
effect which have improved the mimicry after the major genes have become
established. In an extensive series of experiments with both species (Sheppard et
al., in press, and references therein), this is exactly what has been found. The
big, obvious differences between races, such as the presence or absence of the red
radiate marks over the bases of the wings, or the red versus yellow forewing
band, usually turn out to result from single genes of large effect: a round dozen
of these are known in both species (Table 1 ) . The minor genes are of course
J. R. G. TURNER
284
Table 1. Genetics of races of Heliconius melpomene and Heliconius erato
(A) H. rnelpomene
Location
Suriname
Be1t.m
East
Brad
(2)
Upper
Amazon
(3)
(4)
Wh
Wh
Wh
I
I
7
+
+
+
+
+
+
+
+
+
+
F?
+
Tb
Yb
R
Yb
R
D
D
D
+
+
+
F
Or
+
+
F
’
+
C
(8)
Trinidad/
Venezuela
(7)
East
Ecuador
(1)
Wh
Wh
+
7
+
7
+
+
+
+
P
P
B
S
Rr
B
B
P
+
Or
+
Yb
+
+
F
Or
C
+
+
+
F
Or
+
+
Yb
+
Function of gene
White colour of forewing
band
Forewing triangle
Short split forewing
band
Red colour reponds to F
Red forewing band
Yellow forewing band
Broken yellow band
Red u. orange
Forewing cell spot
Yellow hindwing bar
Hindwing rays
Red base to forewing
(B) H. erato
Belh
(2)
Guiana
Bolivia
(4)
(5)
Upper
Amazon
(3)
LYE
Lr”
+
LYE
R
+
R
R
D
D
D
D
+
+
+
Sd
+
+
+
+
P
P
P
Ur
Or
Ur
Or
Ur
Ur
Wh
Cr
Wh
Cr
Wh
Cr
Wh
Cr
Ye
Ye
re
+
+
+
+
+
+
+
P
+
East
Trinidad/ P a n a d /
Ecuador Venezuela Mtxico
(1)
(7)
(6)
+
+
+
Y
+
+
+
+
Y
+
P
Or
Or
P
+
+
+
Y
+
+
Ur
Or
Ur
Cr
Wh
Cr
Wh
Cr
Tr
Yle
Tr
Tr
+
+
St
Ro
+
+
+
+
+
+
East
Brad
(8)
+
+
+
Y
+
P
Or
Ur
Wh
+
+
+
+
Function of gene
Broken forewing band;
yellow forewing line
Hindwing rays
Red base to forewing
Yellow forewing band
Shortened forewing
band
Yellow hindwing bar
Red u. orange
Band on upperside
responds to St and Sd
White forewing band
Hindwing rectangles
and yellow bar
Yellow hindwing bar
and forewing line
Split forewing band
Round tip to forewing
band
+
Indicates recessive (ancestral) allele.
Numbers refer to Fig. 2.
Simplified from Sheppard ct al. (in press) (also Turner, 1981)
hard to pin down for purely technical reasons, but their effects are quite clear in
many cases: for instance, two or more of them remove the big yellow spot from
the centre of the forewing in the Trinidad race of melpomene (7), a single one
removes the last traces of the yellow bar in Trinidad erato (7), after most of it has
been taken away by two major genes, and an unknown number are responsible
for narrowing the hindwing rays of Amazonian melpomene (2), which otherwise
spread out to cover most of the hindwing (numbers are those of races in Fig. 2).
MIMETIC BUTTERFLIES
285
I n short, Mullerian mimicry evolves, as was originally postulated by Poulton
( 1912) and Nicholson ( 1927), in two stages: rough mimicry is produced by a single
large mutation, which causes the less protected species to converge toward the
better protected, following which the species undergo gradual mutual
convergence by minor genetic variation until the mimicry is perfected. But these
two phases are the theories of Marshall and of Dixey. They were not describing
exclusive alternatives a t all, but the beginning and the end of the same process.
ALLOPATRIC OR PARAPATRIC RACE FORMATION? A GEOGRAPHICAL RECONSTRUCTION
OF THE RECENT PAST
The ice ages in the Amazon
We now have the first part of our reconstruction, a model to account for the
adaptive radiation seen within evolving lines of Heliconius: species like melpomene
and erato have undergone divergence because they tend to mimic other
warningly coloured butterflies that fly with them, because these are for some
reason better protected (normally because more numerous or more distasteful),
and, for smaller amounts of divergence, because other less protected species
come to mimic them. What of the history?
According to our model, racial divergence of the kind seen in melpomene and
erato will occur when populations in different areas fly with different wellprotected species; the driving force will be fluctuations in the numbers of
different warningly coloured butterflies in different areas. A formerly rare
species which becomes very common will tend to draw all sufficiently similar
species to its own pattern. However, it cannot do this immediately, as the first
stage in evolution of Mullerian mimicry has to wait for the occurrence of an
appropriate mutation, which in populations as small as those of some forest
butterflies (Ehrlich & Gilbert, 1973) may take a considerable time. Two
populations of Heliconius hermathena fly with the appropriate red-banded race of
erato, but do not mimic it; apparently the mutation has simply not occurred
there (Fig. 3) (Brown & Benson 1977). Thus, evolutionary divergence of this
kind is likely to happen only when the change of abundance lasts for a long
time.
There is now ample evidence that the climatic fluctuations of the Quaternary
had considerable effects on the rain forest habitat of these butterflies, causing
what is now the almost continuous Amazonian selva to be split into more-or-less
isolated patches separated by drier, more open habitats. The arguments for this
have been extensively reviewed by Flenley (1979), and in the recent book edited
by Prance (1982); briefly they are:
(1) Lake sediments from the Andes show that at higher altitudes the climate
became colder and drier, even in the equatorial region, during the glaciations
(Fig. 5).
(2) Soil cores from Amazonia indicate alternations of forest and grassland,
which seem to correlate with the changes seen on higher ground.
(3) A computer simulation of world climate around 18 000 BP, around the last
glacial maximum, showed a world-wide lowering of rainfall, and a cooling of
6 7 ° C in the Amazon Basin (Gates, 1976).
286
,I. R. G. TURNER
Mountoin Deok
Figure 4.Disorderly extinction shown by the distribution of 13 mammal species (shading indicates
presence) on 17 mountain tops in the Great Basin (western U.S.A.).After Turner (1977a), using
data ofJ. H. Brown (1971). Illustrations of the species, and a map, can be found in May (1978).
Disorderly extinction on islandJ
The effect on a fauna of being confined in an island of forest surrounded by
grassland will be the progressive extinction of various of the forest species, as an
isolated patch of habitat supports fewer species than the same area continously
connected. The effect can be seen in the fauna of the boreal forest of the southwestern U.S.A., where this is now isolated on a group of mountain peaks
surrounded by desert (Fig. 4, after data of J. H. Brown, 1971). No mountain
contains the whole fauna, and hardly any two mountains have an identical set
of species, even where the total number is the same. The same must have
happened to the flora and fauna of the Amazonian forest islands in the
Quaternary. The effect on the warningly coloured butterflies would have been
long-term changes in abundance: this would be ensured, even when no butterfly
species became extinct, by the extinction of parasites, predators, host-plants,
competitors, competitors of host-plants, and so on, in the densely packed and
interlocked ecosystem of the rain forest (Gilbert, 1977, 1980). Thus the best
protected, and hence most mimicked, pattern in each refuge would be different.
The disorderly extinction of members of the flora and fauna is an ample cause
for the divergent evolution seen within species of Heliconius.
Several authors (Endler, 1977, 1982; White, 1978; Benson, 1982) have quite
rightly challenged our assumption, when we first proposed that glacial refuges were
an explanation for Heliconiusdivergence(Turner, 1965;Brown, Sheppard & Turner,
1974), that race formation was allopatric. Why, they asked, as no isolating
mechanisms have appeared, should the races have not formed parapatrically, that is
to say, within a continuous population? (This was also the explanation put forward
by Dobzhansky when he first saw the distribution maps of H. melpomene and
MIMETIC BUTTERFLIES
High
I
LOW
17OC
i
Subandean forest
Andean forest
ti
Sub Paramo {
5OC Open grass P o r a m i
mu,uu
/--
\
---
v
Relative
:;y;:‘e;
Vertical movements
of vegetation belts
(and approx chonges
of overage onnual
7
H. erato.) All that is required for parapatric race formation in Heliconius is that there
should be an area of forest within the continuous Amazonian forest in which
some species, rare elsewhere, is common and well-protected. If another species
produces a mutation which mimics this pattern, this mutation will increase in
frequency and spread in space, until it comes to some place in the forest where
the pattern is no longer the best protected; there, its advance will be halted.
Although the particular case of Mullerian mimicry, which has some rather odd
dynamics, has not been fully investigated, there are sound theoretical reasons for
believing that as further modifying genes spread through the new race, these
would be halted a t this boundary and might cause it to show a steep cline in
gene frequency, imitating closely a hybrid zone formed by secondary contact.
Like such a hybrid zone, the cline will tend to form in areas of low population
density, or places where the habitat is not particularly suitable for Heliconius
(Endler, 1977; Barton, 1979).
The parapatric model is thus not at all easy to distinguish from the allopatric
model, which proposes that the races formed inside isolated refuges and that the
gene frequency clines where they meet (which are indeed sometimes at regions
of low density-Turner,
1976) are secondary hybridization zones. Both models
predict the same outcomes, and depend on the same mechanism for the spread
of the new mutation, which must initially spread out ‘parapatrically’ from the
focus where it first occurred, even if this is inside a refuge. The only difference
between them is that in one the new form appears in an isolated patch of
forest, and then spreads out with it once it expands again, whereas in the other
the spread of the gene occurs in a continuously connected area of forest.
As the difference between the models is thus purely one of history, not of
dynamics, our choice between these two historical explanations for the adaptive
radiation of the races of Heliconius melpomene and H . erato will in the end rely on
independent evidence for the existence of refuges: if the forest did break up into
islands, then the Heliconius populations must have been trapped inside them.
The allopatric and parapatric models of race formation appear antithetical
only if we assume that genetical isolation is of crucial importance in starting
racial divergence. But it is well known that genetic differentiation can take place
in the face of quite strong gene flow (e.g. Bradshaw, 1971). If the crucial factor
is a changing faunal balance, as has been argued here, then the allopatric and
parapatric models, far from being antithetical, are simply the ends of a
continuum: no habitat is uniform; all populations tend to be patchy in their
densities, so that even a continuously distributed species has patches of high
J. R. G. TURNER
288
--.
--.
Figure 6 . Amazonian refuges: approximate distribution of areas favourable for rainforest organisms
at a time close to the last glacial maximum at c. 18000 BP, deduced from distributions of various
groups of forest butterflies, especially heliconids, and from palaeoecological data. After Brown
(1977a, 1979).
density surrounded by sparser areas; an isolated refuge is simply the most
extreme case.
What will be different in a refuge is the time for which extinctions persist.
Once a patch of forest becomes isolated, extinct species are unlikely to reappear,
whereas local extinctions in a continuous forest are likely to be reversed within
quite a short time, perhaps tens or hundreds of years. Given the waiting time
required for new mutations, the changes of faunal balance which, I have
argued, are the driving force in race formation in Heliconius, persisting as they
would until the refuge expanded again, and thus lasting for periods which we
MIMETIC BUTTERFLIES
289
know from the palaeobotanical evidence would have been upwards of thousands
of years, would be much more likely to cause race formation when the forest was
fragmented than when it was continuous. Thus although races of Heliconius may
form all the time, they will form more rapidly during periods when the climate
has deteriorated so as to break up the forest and impede the migration of forest
species. This would explain the otherwise puzzling fact that the centres of
distribution of the Heliconius races correspond so well with the refuge centres
deduced by Haffer (1969) from bird distributions, and by Miiller (1973) from
vertebrates in general (Brown et al., 1974; Brown, 1977b).
I n sum, what is proposed is that the Quaternary glaciations caused a
deterioration of the Amazonian rain forest, not necessarily so far as to split it
into completely isolated refuges like those shown in most reconstructions (e.g.
Brown et al., 1974), but to the stage sketched in Fig. 6, where migration and
recolonization by forest organisms became much impeded by more open
habitats in the drier parts. The changing faunal balance, which resulted from
haphazard extinctions in different parts of the forest, then caused changes in the
abundance of butterfly species, which in turn caused other butterflies to evolve
new patterns mimicking the locally best-protected species. When the climate
improved, the new races became largely continuous and contiguous, producing
rather sharp contact zones between them, and giving the pattern of race
distribution which we see today (Fig. 2). This reconstruction belongs strictly
neither to the allopatric nor parapatric systems.
GRADUALISM O R PUNCTUATION? A PHYLETIC RECONSTRUCTION
Switching niches
Evolutionary novelty is one of the outstanding challenges to evolutionary
(particularly Darwinian) theory: how can a new, necessarily imperfect
adaptation appear when it would disrupt an adaptation perfected by millenia of
natural selection? (See, for example, Frazetta, 1975.) Mimicry provides one
answer. O n those rare occasions when the environment has changed in such a
way that the new, necessarily imperfect, adaptation produced by a new
mutation is in fact fitter than the old perfected adaptation, then an evolutionary
novelty will appear. After the initial crudely adapted mutation has spread, this
new phenotype will itself be perfected by the selection of other modifying genes.
This model has been exemplified here by the evolution of mimicry in Heliconius
(for another Mullerian mimic, a g a e n a ephialtes, see Sbordoni et al., 1979; for
Batesian mimicry see Sheppard, 1962, 1975 and Turner, 1977c) but there is no
reason why the same should not be true of other adaptations as well, and this
gives us some kind of a general description of adaptive evolution. Organisms will
tend to dig themselves deeper and deeper into their own ecological niche; slow
changes in the environment may produce slow evolutionary responses in the
organisms, but otherwise evolution will be very conservative. However, if an
ecological niche becomes emptied by extinction (the equivalent of a warning
pattern becoming very common), then a species which can produce a single
mutation giving poor, but adequate adaptation to that niche, can come to
occupy it. I n this way, quantum jumps, within the limits of what can be
achieved by the mutation of single genes, will occur in evolution, and they will
be particularly likely to occur on islands of all sorts (whether new, empty islands
I5
290
J. R. G. TURNER
being colonized, or refuges carved from a formerly continuous habitat) where
extinction or failure to colonize leave niches empty for long periods (see Turner,
1977a, 1982).
A Mullerian mimicry ring is of course a rather simplified analogue for an
ecological niche, for as far as we can judge a warning pattern is subject simply
to normalizing selection, whereas many of the characters responsible for the
overall adaptation of the organism to its environment will be subject to a
mixture of normalizing selection exerted by competition with the species that
are packed ‘next’ to it in the niche space, and disruptive selection caused by
intraspecific competition (which gives an advantage to individuals which
deviate from the norm of their own species). It must be the balance between
these forces which determines the overall form of a species, and sets the
boundaries of what it can and cannot do.
Estimating the ancestors
The natural question in the present intellectual climate: “have we produced an
explanation for the punctuated equilibrium system?”, recently acclaimed as
having defeated neo-Darwinism (Lewin, 1980; Gould, 1980), can be
investigated with my last piece of reconstruction: the evolutionary tree of
melpomene and erato.
We can set up two hypotheses to explain the parallel variation of melpomene
and erato: (1) starting with some very different patterns, the two species have
converged, to produce the present set of parallel, mimetic races; (2) starting
with similar, perhaps mutually mimetic patterns, the two species have
undergone a parallel adaptive radiation, mimicking each other all, or most of,
the time. The second hypothesis is the more likely, and we can test it, for we
have a theorem in population genetics that allows us to reconstruct the ancestral
pattern of a species. Haldane (1924) was the first to point out that if two
mutations have the same adaptive effect (i.e. the same selective value), then if
one is dominant and the other recessive, the dominant one has the
overwhelmingly better chance of becoming established in the population. This is
because the dominant mutation rises rapidly in frequency from the start,
whereas the recessive, virtually never appearing in a homozygote when still rare,
is effectively protected from the action of natural selection, and remains rare for
a very long time. Under some circumstances a dominant mutation appearing
after a recessive has started to spread, can even beat it to the winning post by
causing the recessive to decline in frequency again (a result which surprises most
population geneticists when they first meet it!) (Fig. 7). The long-term effect of
this phenomenon, which I have called ‘Haldane’s sieve’, will be that most of
the genes which are fixed in populations by natural selection will be those which
are dominant in effect.
Therefore the simple rule is that dominant genes tend to be derived, and
recessive genes ancestral: if we take all the recessive alleles that we know in a
species, then the pattern they produce will be rather close to the ancestral
pattern. It may, of course, not actually be the ancestral pattern, as on rather
rare occasions a recessive gene may be substituted for a dominant one, but it is
the closest we can get to the ancestral pattern, in the sense that were we to put
one dominant gene in there, the chance that we had correctly identified the
29 1
MIMETIC BUTTERFLIES
300 2000
Figure 7. Part of the working of Haldane's sieve: a dominant gene (d) becomes established in a
population much more easily than a recessive (r). I n this computer simulation the frequencies
(vertical axis) of three alleles at the same locus under selection are shown over time (horizontal
axis). Both the new alleles ( d and r) are at the same advantage over the original wild-type ( ) and
differ only in that d is fully dominant and r fully recessive. Allele r is given a head start and would
increase to loo%, as shown by the dotted line, if allele d were not introduced at very low frequency
at generation 0; then d rapidly increases in frequency, forcing r to go into reverse, and forcing it to a
low equilibrium frequency as the wild-type is finally eliminated.
+
exceptional case would be rather small, with the result that the pattern would
now be incorrect in two features instead of in one. Our surprise when we
reconstructed the ancestors of melpomene and erato in this way was considerable
(Sheppard et al., in press): not only were these ancestors mimetic, as we have
noted is the most likely explanation of the extraordinary parallel mimicry of
their descendants; they turn out to be butterflies with black and yellow bars,
with not a trace of red (which would I think be difficult for anyone to guess by
looking at the array of patterns now presented by the species). Yet these yellowbarred patterns are found also in two close relatives, one of melpomene and the
other of erato, which being non-mimetic (although they look so similar, their ranges
are separated by thousands of miles, and no other sympatric Heliconius or
ithomiid resembles either of them) are likely to have evolved rather more slowly
and therefore to have a pattern closer to the ancestor. With four independent
lines of evidence (two independent reconstructions from the genetics, and two
related species) all pointing in that direction, it is difficult to avoid the
conclusion that the ancestors of both species were mutual mimics, black with
yellow stripes (Fig. 8).
A similar method has already been successful, although not entirely
unambiguous, in reconstructing the sequence of evolution in Papilio dardanus
(Sheppard, 1962; Vane-Wright, 1979, 1980).
Evolutionary trees
The same method can be used to reconstruct the common ancestor of any
pair of races by taking all the recessive alleles contained in either or both of
the races, and from this it is not difficult to construct the most parsimonious
evolutionary tree: one simply connects together those pairs of races which have
15'
292
J. R. G. TURNER
Figure 8. Cladograms suggesting parallel evolution of Heliconius rnelpomene (left) and H. erato (right).
The patterns of forms a-d, which are reconstructed hypothetical ancestors of the existing races
shown at the top, are still represented by the relict forms, mostly non-mimetic, of other species:
the largest numbers of dominant alleles in common, reconstructs their common
ancestors, and then repeats the process by joining these to their closest partners,
until the tree is complete. Those versed in cladistics will recognize this as the
weighted invariant step strategy (WISS) of Farris, Kluge & Eckardt (1970); the
only arbitrary axioms, apart from knowing which are the ancestral alleles, are
that only non-ancestral characters give information about the evolutionary tree,
or (its strict equivalent in this case) that the most parsimonious tree is the best
obtainable estimate of the real tree, and that reversals of evolution (the
substitution of the ancestral recessive allele) do not take place.
This method, applied to the genetic constitutions of the races of melpomene and
erato (Table 1) gives two alternative minimum length trees, which interestingly
enough have the same topology in both species. First, there is a two-phylad tree,
with one main branch bearing the Amazonian races, and the other bearing all
those races found outside the Amazon basin. Although not impossible, this type of
tree seems unlikely to be correct, as this second group of races are widely spread
from Central America to southern Brasil, and practically encircle those in the
Amazon basin; it is hard to imagine a sequence of events in space and time
which would fit this type of tree into the geographical distributions. Second,
there is a series of three-phylad trees in which there are two widely-spread
branches ending in various extra-Amazonian races, with the Amazonian races
coming off one of these branches (Fig. 8 ) . This is a much better fit to the
geographical pattern. Within this topology one can, without increasing the
length of the tree in either species, permute the positions of the extra-Amazonian
races: I have chosen the one shown in Fig. 8, as it is necessary to make some
MIMETIC BUTTERFLIES
293
g;f#J
....:.*....,
.:::/.:.,
......A
A..
A. H. nattereri; B, H. timareta, C , H . eleuatus roraima; D. H. hermathena, see also Fig. 3. Cross bars
denote substitutions of the major genes. Existing races are those shown in Fig. 2 as numbers (left to
right, upper row first) 2, 7; I , 3, 4,8 (melpomene) and 2, 4, 7; 1, 3, 5 , 6 , 8 (erato).
choice by way of example, because it complies best with some further genetic
information which for various reasons could not be included in the data matrix
(Table l ) , and because this arrangement produces at all the major nodes,
ancestral patterns which are still found in races of other species of heliconius, all of
them probably now non-mimetic and very restricted in geographical
distribution, which may possibly be relics of the mimicry rings to which
melpomene and erato belonged at these times (Fig. 8, B, C, D).
For the present purpose, however, it is not important to know just how closely
the estimated phylogeny resembles the real one, nor which of the alternative
minimum trees is the most likely. What is certain is that the course of evolution
in both species was something like Fig. 8 , with the species probably remaining
mutual mimics most of the time. In each branch of the tree a comparatively
small number of gene substitutions (shown by the cross-bars) has taken place;
perhaps rather surprisingly in view of the present diversity of the patterns, but
in complete accord with our dynamic model, no really drastic alteration of the
pattern is required at any stage. One, two, or three mutations usually suffice.
We do not of course know, when there are two substitutions, whether one is the
major initial mutation and the other a modifying gene brought in as the
immediate result* or whether we are seeing the remains of two evolutionary
*There is some confusion over the word ‘modifier’ (Rothschild, 1981); this is not a synonym of ‘polygene’,
but a gene which modifies or improves the rough mimicry produced in the initial stage of evolution, being in
some cases a detectable single mutation, or what in classical genetics is called a ‘major gene’. Thus, in the
moth a g a e n a ephialtes, Sbordoni el al. (1979) have convincingly argued that the pattern was altered first by a
major change in pigment distribution, and second by changing the few remaining red marks to yellow. This
latter change, produced by a ‘major’ mutation in the pigment synthesizing equipment is, in terms of the
Poulton-Nicholson model, a ‘modifier’ of the mimicry produced by the first mutation.
294
J. R. G. TURNER
steps, but however we spread the mutations out it is most unlikely that they
produced continuous evolutionary change during the time covered by the tree.
For a dominant mutation with only a 1% selective advantage will travel from
the point where only one butterfly in a thousand has the new pattern to the
point where only one in a thousand has the old one (and both collectors of
Heliconius, who would probably attribute the oddity to gene migration from the
neighbouring race, and palaeontologists would tend to regard a population as
uniform with this or any lower frequency) in less than 4000 generations*. (It is
anybody's guess just what the selective advantage is, although from the values
obtained for visual predation on moths in England (Kettlewell, 1973), 1% is a
low estimate; the time required is in linear inverse proportion to the advantage,
so that selection five times as strong would take one-fifth of this time.)
Heliconius have up to 10 generations a year, and it is reasonable to suppose
that the evolutionary trees cover the span of at least 30000 years occupied by
the most recent glacial cycles (Fig. 5 ) . Hence with each substitution taking as
little as 400 years, for much of their history the populations of melpomene and
erato must have presented an almost constant, unaltered phenotype. Indeed, if
they were in a state of continuous change we would not expect to find the stable,
widely distributed phenotypes which we see today; even in those Heliconius
which are polymorphic (e.g. H . doris) we seem to be dealing with a stable
polymorphism rather than with gene substitution, for eighteenth century
illustrations show that the polymorphism has persisted for at least 200 years, or
for over 2000 generations (Turner, 1967).
Evolution
jerks
Does this reconstruction allow us to choose between the currently canvassed
theories of phyletic grandualism and punctuated equilibrium? T h e alternation
of long periods with a stable phenotype, separated by what was probably quite
a rapid period of gene substitution, certainly does not sit well with the idea of
uniform slow evolution. But it does not correspond well with the punctuated
equilibrium theory propounded by Eldredge & Gould (1972) either.
According to this model, the transitions from one stable form to another are
produced by rapid allopatric speciation in small peripheral populations. The
changes seen in the present evolutionary trees are occurring in refuge
populations within the main range of the species, not in small peripheral
isolates, and although allopatric, they are not associated with speciation, as no
speciation has taken place (the races can and do hybridize where they meet). I t
is unlikely even that the changes are immediately associated with branching
points (they will be delayed until the appropriate ecological and genetic changes
have taken place after the refuges are formed). They could obviously take place
'From the equations of Haldane (1924) it is not difficult to show that the number of generations for the
phenotype produced by a single dominant gene to change in frequency from lo-" to 1-10-' (e.g. from 0.001
to 0.999) is given by the formula:
t = (10"'*+3.45x+0.69)/s,
where s is the coefficient of selection in favour of the new phenotype. In the present case, x = 3, so that
1 = 42.66/s. If s were 0.01 (a 1 % advantage), then 4266 generations would be required. But selection on a
Miillerian system is positively frequency-dependent, so that s will actually increase during the period of genesubstitution. This will have the effect offurther accelerating the speed ofevolution, by an amount which will be
a rather complicated function of the abundance of the evolving species and both the mimicry rings to which it
belongs. The reduction below 4000 generations might be substantial.
MIMETIC BUTTERFLIES
295
without any branching at all, for a species which occupied only a single refuge,
having become extinct in all others, could just as readily suffer a radical
alteration in its pattern; an essential feature of the punctuated equilibrium
model, that the original stable phenotype becomes extinct and is replaced with a
new one evolved elsewhere, is not met.
It is apparent, therefore, that jerky, rather than smooth evolution of the
colour patterns is taking place, but that this is happening within more-or-less
large, and more-or-less central populations, and that it is associated with
changes in the ecology of those populations rather than with the cycle of genetic
isolation, allopatric speciation, extinction and recolonization required by the
punctuated equilibrium model (Stanley, 1979).
EVOLUTION: AN OLD AND GENERAL THEORY
A dedicated supporter of Richard Goldschmidt would object that what has
been said so far has nothing to do with evolution beyond the level of the species,
which Goldschmidt maintained was governed by processes different from
infraspecific evolution (Gould, 1980). It is a criticism still validly made of
experimental population genetics, that its findings may be inapplicable to
evolution in the long term.
There are two more-or-less direct lines of evidence that in Heliconius the events
which occur within species also account for the pattern generated over a much
longer time (it would perhaps be cheeky to describe what may have taken only
a few hundred thousand years as macroevolution). First, the genetic changes
within species appear to be the same as some of the differences between species
(a finding which is of course extensively confirmed by molecular biologists).
Figure 9 shows that most of the pattern of Heliconius ethilla can be produced by
an appropriate combination of the genes already known in H. melpomene, its close
relative. Second, the pattern of parallel mimicry seen between the races of
Figure 9. The superficially very different pattern of Heliconius ethilla (left) can be derived rather
easily from a pattern of Heliconiur mclpommc (right) produced by the genes D , R, 6 , NN, Yb, Wh, t, or,
F, c plus the polygenes which widen the hindwing rays. As these genes are all known from various
races of H. melpomcne (see Figs 2 & 8), this strongly suggests that the same sorts of genetic change are
involved in both trans-specific and infra-specific evolution.
MIMETIC BUTTERFLIES
297
melpomene and erato (and the races of a further half dozen species which are their
co-mimics) is repeated at the next taxonomic level in the form of parallel
mimicry between series of species within subdivisions of the genus (Table 2).
Whatever events led to the parallel mimicry between the races must have been
repeated several times (as, of course, glacial cycles did), the geographical races
generated in earlier cycles having now become full species. There is every reason
to suppose that what we have discovered with Heliconius melpomene and H . erato
lies at the root of a much longer term evolutionary pattern.
What is more, this pattern, as can be seen from the arrangement of taxonomic
groups and colour patterns in Table 2, is the classic one of adaptive radiation
(within groups into different patterns) and convergence (between groups into
the same pattern). What have we learned, in this case, about this standard,
widespread evolutionary process?
It occurs, under natural selection, as a result of the adaptation of populations
to different ecological niches (in this case different mimicry rings). A quite
radical change of niche can occur, accompanied by an extensive change in
phenotype, provided that a single mutation can produce an adequate
adaptation to the new niche, that is to say provided the necessarily initially poor
adaptation gives the new mutation greater fitness than the original allele. As
this will not often happen, evolution will tend to conservatism, with roughly
constant phenotypes being maintained for long periods. But changes will be
likely to occur if ecological niches become vacant, as they often will when a
fauna and flora is split into refuges by deteriorating conditions, or during the
colonization of new, empty habitats. I t is the cycle of extinction and
colonization which drives this process rather than the stoppage of gene flow
itself. Once the new mutation (which is usually dominant) becomes established,
then further improvements in its adaptation are made by further modifying
genes, and it becomes itself the bearer of a well adapted conservative phenotype
until the next cycle. Although this process conforms superficially to the
punctuated equilibrium model, it differs from it in several important respects,
particularly in not being associated with speciation. In fact, it is becoming clear
from a number of studies (B. J. Turner, 1974; Sene & Carson, 1977; Scanlan,
Maxson & Duellman, 1980) that speciation, morphological and molecular
evolution are not highly correlated, and we have shown that the ‘jerky’
evolution of the colour patterns in Heliconius is accompanied by ‘gradualistic’
evolution at the molecular level (Turner, Johnson & Eanes, 1979).
In sum, we have (1) evolution by the selection of large mutations and
modifiers (two-phase evolution), (2) driven by the extinction cycle (the stoppage
of ‘fauna flow’ and the vacation of ecological niches), within large, central
populations, (3) producing an evolutionary history at the phenotype level which
is not uniform and gradual but jerky.
In drawing these conclusions I have of course rejected a number of alternative
descriptions of evolution (the major mutations are not ‘hopeful monsters’ for
example, neither can I convince myself that evolution has been uniform and
gradual). One cannot have ‘pluralism’ in one’s approach (Gould & Lewontin,
1979), in the sense of simultaneously believing six incompatible explanations
before breakfast. But I have tried to show that the difficulty with adversary
science is in setting up the hypotheses between which one is to choose; by using
an inquisitorial method, I have,argued that in three cases (gradual u. saltational
J. R. G. TURNER
298
evolution, parapatric u. allopatric race formation, and gradualism u. punctuated
equilibrium) we are ill advised to select one or other of the choices on offer: the
most constructive model is somewhat like a synthesis of the two. This synthesis
(propounded to this Association many years ago in a discussion of Batesian
mimicry-Sheppard,
1962) is that of Mendelian genetics, Darwinian theory,
ecology, systematics, and historical biogeography. Its familiar name is neoDarwinism.
REFERENCES
BARTON, N. H., 1979. The dynamics of hybrid zones. Heredity, 43: 341-359.
BENSON, W. W., 1972. Natural selection for Mullerian mimicry in Heliconius erato in Costa Rica. Science, 176:
936-939.
BENSON, W. W., 1982. Alternative models for infrageneric diversification in the humid tropics: tests with
passion vine butterflies. In G . T. Prance (Ed.), Biological DiversiJication in the Tropics: 608-640. New York:
Columbia University Press.
BRADSHAW, A. D., 1971. Plant evolution in extreme environments. In E. R. Creed (Ed.), Ecological Genetics
and Evolution: 20-50. Oxford: Blackwells.
BROWN, J. H., 197 1. Mammals on mountain tops: nonequilibrium insular biogeography. American Naturalist,
105: 467-478.
BROWN, K. S. Jr, 1977a. Centros de evoluGio, refiigios quaternirios e conservaG8o de patrimbnios gentticos
na regiHo neotropical: padr6es de diferenciaGHo em Ithomiinae (Lepidoptera: Nymphalidae). Acta
Amazonica, 7: 75-137.
BROWN, K. S., Jr, 1977b. Geographical patterns of evolution in neotropical forest lepidoptera
(Nymphalidae: Ithomiinae and Nymphalinae-Heliconiinae). In H. Descimon (Ed.), Bioglographie et
Evolution en AmCriquc Tropicale: 118-160. Paris: Publications du Laboratoire de Zoologie de 1’Ecole Normale
Superieure, No. 9.
BROWN, K. S., Jr, 1979. Ecologia geogrdjca e evolu@ nas florestas neotropicais. Livre Doctncia thesis,
Universidade Estadual de Carnoinas.
BROWN, K. S., Jr, 1981. The biology of Hcliconius and related genera. Annual Review of Entomology, 26:
427456.
.- . .- .
.
BROWN, K. S., Jr & BENSON, W. W., 1977. Evolution in modern Amazonian non-forest islands: Heliconius
hermathena. Biotropica, 9: 95-1 17.
BROWN, K. S., Jr, SHEPPARD, P. M. & TURNER, J. R. G., 1974. Quaternary refugia in tropical
America: evidence from race formation in Heliconius butterflies. Proceedings of the Royal Society, B , 187:
369-3 7 8.
DIXEY, F. A., 1896. On the relation of mimetic patterns to the original form. Transactions of the Entomological
Society of London, I&%, 65-79.
DIXEY, F. A,, 1907. On the diaposematic resemblance between Huphina corua and Ixias baliensis. Transactions
of the Entomological Society of London, 1906, 52 1-524.
DIXEY, F. A., 1909. On Miillenan mimicry and diaposematism. Transactions of the Entomological Society of
London, 1908, 55S583.
DUNCAN, C. J. & SHEPPARD, P. M., 1965. Sensory discrimination and its role in the evolution of Batesian
mimicry. Behaviour, 24: 269-262.
EHRLICH, P. R. & GILBERT, L. E., 1973. Population structure and dynamics of the tropical butterfly
Heliconius ethilla. Biotropica, 5: 69-82
ELDREDGE, N. & GOULD, S. J., 1972. Punctuated equilibria: an alternative to phyletic gradualism. In J.
Ma Schopf (Ed.), Models in paleobiology. San Francisco: Freeman, Cooper & Co.
ENDLER, J. H., 1977. Geographic Variation, Speciation and Clines. Princeton, NJ: Princeton University Press.
ENDLER J. H., 1982. Pleistocene forest refuges: fact or fancy? In G. T. Prance (Ed.), Biological DiversiJication
in the Tropics: 641-657. New York: Columbia University Press.
FARRIS, J. S., KLUGE, A. G. & ECKHARDT, M. J., 1970. A numerical approach to phylogenetic
systematics. Systematic ~ o o l o g y 19:
, 172-191.
FLENLEY, J., 1979. The Equatorial Rain Forest: A Geological History. London & Boston: Butterworths.
FRAZETTA, T. H., 1975. Complex Adaptations in Evolving Populations. Sunderland, MA. Sinauer.
GATES, W. L., 1976. Modeling the ice-age climate. Science, 191: 1138-1144.
GILBERT, L. E., 1977. The role of insect-plant coevolution in the organization of ecosystems. In V. Labrie,
(Ed.), Comportment des Insectes el Milieu Trophique. Colloques Internalionaux, C N R S , 265: 399-41 3. Paris.
GILBERT, L. E., 1980. Food web organization and the conservation of neotropical diversity. In M. E. Soult
& B. A. Wilcox (Eds), Consmuation Biology: 11-33. Sunderland, MA: Sinauer.
GOODALE, M. A. & SNEDDON, I., 1977. The effect of distastefulness of the model on the predation of
artificial Batesian mimics. Animal Behaviour, 25: 660-665.
MIMETIC BUTTERFLIES
299
GOULD, S. J., 1980. Is a new and general theory of evolution emerging? Palaeobiology, 6 : 119-130.
GOULD, S. J. & LEWONTIN, R. C., 1979. The spandrels of San Marco and the Panglossian paradigm: a
critique of the adaptationist programme. Proceedings of the Royal Society of London, B , 205: 581-598.
HAFFER, J., 1969. Speciation in Amazonian forest birds. Science, 165: 131-137.
HALDANE, J. B. S., 1924. A mathematical theory of natural and artifical selection. Part I. Transactions of the
Cambridge Philosophical Society, 23: 19-41,
HAMMEN, T . VAN DER, 1974. The Pleistocene changes of vegetation and climate in tropical South
America. journal of Biogeography, 1: 3-26.
KETTLEWELL, H. B. D., 1973. The Evolution of Melanism. The Study of a Recurring Necessity. Oxford:
Clarendon Press.
LEWIN, R., 1980. Evolutionary theory under fire. Science, 210: 883-887.
MARSHALL, G. A. K., 1908. On diaposematism, with reference to some limitations of the Miillerian
hypothesis of mimicry. Transactions of the Entomological Society of London, 1908, 93-142.
MARSHALL, G. A. K., 1909. Birds as a factor in the production of mimetic resemblances among butterflies.
Transactions of the Entomological Society of London, 1909, 329-383.
MAY, R. M., 1978. The evolution of ecological systems. In Evolution. A ScientiJc American Book: 80-90. San
Francisco: Freeman.
MOULTON, J., 1909. On some of the principal mimetic (Miillerian) combinations of tropical American
butterflies. Transactions of the Entomological Society of London, 1908, 585-606.
MOLLER, P., 1973. The Dkpersal Centres of Terrestrial Vertebrates in the Neotropical Realm
(Biogeographica Vol. 2). The Hague: Junk.
NICHOLSON, A. J., 1927. A new theory of mimicry in insects. Australian <oologist, 5: 1&104.
PAPAGEORGIS, C., 1975. Mimicry in neotropical butterflies. American Scientist, 63: 522-532.
PERKINS, R. C. L., 1912. The colour-groups of the Hawaiian wasps, etc. Transactions of the Entomological Society
of London, 1912, 677-701.
PLOWRIGHT, R. C. & OWEN, R. E., 1980. The evolutionary significance of bumble bee color patterns: a
mimetic interpretation. Evolution, 34: 622-637.
POULTON, E. B., 1912. Darwin and Bergson on the interpretation of evolution. Bedrock, I(1): 48-65.
PRANCE, G. T. (Ed.), 1982. Biological Diversification in the Tropics. New York: Columbia University Press.
ROBINSON, R., 1971. Lepidoptcra Genetics. Oxford & New York: Pergamon.
ROTHSCHILD, M., 1981. Mimicry, butterflies and plants. Symbolae botanicae upsalicnscs, 22(4): 82-99.
SBORDONI, V., BULLINI, L., SCARPELLI, G., FORESTIERO, S. & RAMPINI, M., 1979. Mimicry in
the burnet moth a g a e n a ephialtes: population studies and evidence of a Batesian-Miillerian situation.
Ecological Entomology, 4 : 83-93.
SCANLAN, B. E., MAXSON, L. R. & DUELLMAN, W. E., 1980. Albumin evolution in marsupial frogs
(Hylidae: Gastrothcca). Evolution, 34: 222-229.
SENE, F. M. & CARSON, H. L., 1977. Genetic variation in Hawaiian Drosophila. IV. Allozymic similarity
between D . silvestris and D. heteroncura from the island of Hawaii. Genetics, 86: 187-198.
SHEPPARD, P. M., 1962. Some aspects of the geography, genetics, and taxonomy of a butterfly. In Taxonomy
and Geography: 135-152. London: Publication No. 4, Systematics Association.
SHEPPARD, P. M., 1975. Natural Selection and Heredib, 4th ed., London: Hutchinson.
SHEPPARD, P. M., TURNER, J. R. G., BROWN, K. S., jr, BENSON, W. W. & SINGER, M. C., (in
press). Genetics and the evolution of Muellenan mimicry in Hcliconius butterflies. Philosophical Transactions
of the Royal Society of London, B.
SIMS, R. W., PRICE, J. H. & WHALLEY, P. E. S., 1983. Evolution, Time and Space. The Emergence of the
Biosphere. London and New York: Academic Press.
STANLEY, S. M., 1979. Macroevolution. Pattern and Process. San Francisco: Freeman.
TURNER, B. J., 1974. Genetic divergence of Death Valley pupfish species: biochemical versus morphological
evidence. Evolution, 28: 28 1-294.
TURNER, J. R. G., 1965. Evolution of complex polymorphism and mimicry in distasteful South American
butterflies. Proceedings of the XI1 International Congress of Entomology, 1964, 261.
TURNER, J. R. G., 1967. Some early works on heliconiine butterflies and their biology (Lepidoptera,
Nymphalidae). journal of the Linnean Society, London (<oology), 46: 255-266.
TURNER, J. R. G., 1971. Two thousand generations of hybridisation in a Heliconiur butterfly. Evolution, 25:
471482.
TURNER, J. R. G., 1975. A tale of two butterflies. Natural History, 84 (2): 28-37.
TURNER, J. R. G., 1976. Muellerian mimicry: classical ‘beanbag’ evolution and the role of ecological islands
in adaptive race formation. In S. Karlin & E. Nevo (Eds), Population Genetics and Ecology: New York &
London: Academic Press. 185-2 18.
TURNER, J. R. G., 1977a. Forest refuges as ecological islands: disorderly extinction and the adaptive
radiation of muellerian mimics. In H. Descimon (Ed.), Bioglographie et Evolution en Amirique Tropicale:
98-117. Paris: Publications du Laboratoire de Zoologie de l’Ecole Normale Supkrieure, No. 9.
TURNER, J. R. G., 1977b. A Bibliography of Heliconius and the Related Genera: 1-21. Stony Brook, NY:
Program in Ecology and Evolution contribution, No. 151.
TURNER, J. R. G., 1977~.Butterfly mimicry: the genetical evolution of an adaptation. In M. K. Hecht, W.
C. Steere & B. Wallace (Eds) Evolutionary B i o l o u , 10: 163-206. New York: Plenum.
300
J. R. G. TURNER
TURNER, J. R. G., 1981. Adaptation and evolution in Heliconius: a defense of neoDarwinism. Annual Review
of Ecology and Systematics, 12: 99-121.
TURNER, J. R. G., 1982. How do refuges produce biological diversity? Allopatry and parapatry, extinction
and gene flow in mimetic butterflies. I n G . T. Prance (Ed.), Biological Diversification in the Tropics: 309-335.
New York: Columbia University Press.
TURNER, J. R. G . ,JOHNSON, M. S. & EANES, W. F., 1979. Contrasted modes of evolution in the same
genome: allozymes and adaptive change in Heliconius. Proceedings of the National Academy of Science, US.
A,,
76: 19241928.
VANE-WRIGHT, R. I., 1979. Towards a theory of the evolution of butterfly colour patterns under
directional and disruptive selection. Biological Journal of the Linnean SocieQ of London, 11: 141-152.
VANE-WRIGHT, R. I., 1980. A classification of sexual interactions, and the evolution of species-specific
coloration in butterflies. Nota lepidopteralogica, 3: 91-93.
WHITE, M. J. D., 1978. Modes of Speciation. San Francisco: Freeman.