Adaptation and Evolution in Heliconius. A Defense of NeoDarwinism

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A Defense of NeoDarwinism
John R. G. Turner
Departmentof Genetics, University of Leeds, LeedsLS29JT, England
EVOLUTION AND NOVELTY

The neoDarwinian theory of evolution (or "modemsynthesis") may not
explain evolution in the long term. In particular, it has been suggested that
it explains neither the discontinuities in the fossil record [see reports on the
recent conference in Chicago(68, 71a)], nor the origin of complex, inte-
grated adaptations (49, 90). To study such matters we must find a group
in which we can investigate the genetics and ecology of present day popula-
tions, as well as evolutionary trends extending over as long a period as
possible: In the absence of a mimetic drosophiloid snail with polytene
chromosomes and an extensive fossil record, and until molecular evolution-
ists can resolve the controversy over just whichaminoacid substitutions are
selected and which are neutral, we must make do with organisms that have
only someof the required properties. The extensive study of the Hawaiian
Drosophila is well known,but has not yet directly addressed the question
posed here; however, an elegant study (34) showed that changes over
period of around 8000years in populations of the snail Cepaea(as revealed
by semi-fossilized shells) could be well accounted for by (a) the selective
effects of temperature knownto act on the forms in present day populations,
and (b) the independently knownfluctuations of the British climate during
that time.
In the genus Heliconius, the passion flower or passion vine butterflies, we
can also investigate such matters, for our combinedknowledge of their
adaptation, ecology, genetics, and phylogenyand of the history of the South
Americanrain forests where they live allows us to bridge the gap between
population genetics and long-term evolution. In this review, I address pri-
99
0066-4162/81/1120-0099501.00
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100 TURNER
madly the question whether the synthetic theory of population genetics,

ecology and evolution supplies a sufficient explanation of what we find.
The omission of a paper from the present bibliography is not intended
as a criticism; for others, see the general review of Heliconius biology (23)
and the comprehensive bibliographies (22, 105). There has always been
free exchange of data and ideas amongHeliconius researchers, and some:
important discoveries and ideas have occurred simultaneously and indepen-
dently; somefoundation work is in unpublished theses (3, 22, 50, 51, 76,
85, 94).
COEVOLUTION AND ECOLOGY
G. E. Hutchinsons bon mot "the ecological theatre and the evolutionary

play" begs the question "Howcan we know the dancer from the dance?"
The structure of the ecosystem is determined by the evolutionary history
of the species that belong to it. The pressures that makespecies evolve are
produced by their relationships one to another within the ecosystem.
Special Adaptations in Heliconius

The heliconiine butterflies of South AmericaI have diverged both morpho.-
logically and in manyfeatures of biology from the fritillary and checkerspo~
butterflies of the Holarctic, whichare their closest relatives; as their more
exceptional (exceptional, that is, amongbutterflies) adaptations are most
strongly developed amongthe forest-dwelling Heliconius and least among
the open-country and over-the-canopy groups (Dione, Agraulis, Dryas),
they appear to have evolved as a response to the particular ecology of the
tropical rain forests, to their hosts, competitors, predators, and parasites,
as well as to the physical environment. Thus the open-country butterflies
have orange (the predominantcolor), black, and silver fritillary markings;
have normal-shaped wings; are vagile and migratory (4), although they
tend to hometo the host plant wherethey grewup (31); are solitary in theil~
behavior; are only moderately distasteful (15); show an early peak of egg-
laying and then age rather rapidly (40); feed on nectar; lay their eggs on the
older parts of the host-plants; respond only to general visual cues when
searching for host plants (31); and showgenerally rather low,grade mimicry.
of their close relatives only.
~Thegeneric taxonomyof the species discussed is: Agraulis (one sp. vanillae), Dione (juno
plus 2 other spp.), Dryas(one sp. Julia), Dryadula(one sp. phaetusa) and Heliconius (all other
spp.), divided into 4 subgenera, the small, less specialised Eueides, the large (both physically
and numerically) Heliconius, and two smaller groups, Laparus (one sp. doris) and Neruda
(aoede plus 2 other spp.) (20, 104). The highly divergent genus Philaethria maybe more
closely related to the Cethosia group of tropical Asia.
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DARWINIANEVOLUTIONOF HELICONIUS 101
The forest-dwelling Heliconius (subgenus Heliconius) are predominantly

black, with brilliant blue, red, orange, yellow, and white warningpatterns
on exceptionally elongated wings; showrestricted homeranges (29, 41, 71,
98,); have highly developed social behavior in the form of communalroost-
ing (37, 65, 98, 102, 120), cooperative egg-laying (71, 99), and the education
of youngerbutterflies (56); are strongly distasteful (15); are long-lived
adults, with steady, continuousegg production throughoutlife (39, 40); feed
on pollen (53) [pollen and bird droppings in one species (71)]; have elabo-
rate behavioral mechanismsrelated to laying eggs only on the youngest
growth of their host plants (8, 101); are thought to form quite accurate
search images for the shapes of the host plant leaves (54); and showexten-
sive and (to the beginner) bewilderingly accurate mimicryof each other and
of other butterflies, which cuts right across taxonomicgroupings (23, 97,
104).
The other subgenera have developed these specializations to a lesser
degree: Eueides and the open-country genus Dryadula roost communally
(73, 102) but use older parts of their host plants and feed not on pollen but
on bird droppings (19, 102).
Butterfly-Plant Relationships
The specialized features of Heliconius form an intricately interlocking set
of adaptations that in the course of evolution can be expected to enhance
one another, and to enhance and be enhanced by the evolutionary changes
they induce in the other species with which Heliconius interacts in the
ecosystem(Figure 1). It is ditticult to knowwhereto begin in describing this
kind of ongoingchicken and egg (or dancer and dance) situation. The fact
that no heliconiine feeds on any foodplant outside the Passifloraceae (pas-
sion flowers) is a strong reason for believing that the start of it all was the
adaptation of someancestral butterfly to feeding on these plants, probably
by developing a defense against their alkaloids and cyanogenic glycosides
(14). The considerable success and adaptive radiation of the passion vines
(up to 500 neotropical species) and the relative lack of competition from
other herbivores---only some flea-beetles, a family of moths, and some
coreid bugs (which can however inflict severe damageto the parts of the
plants used by Heliconius) have successfully cracked the plant defenses (59)
--presented the heliconiines with a vast ecological opportunity (8). But
the sametime, to exploit this niche, the heliconiines had to solve a series
of evolutionary problemsset by the physical environmentof the rain forest
and by the further defenses developed by the host plants.
The rain forest itself presents a physically intricate environmentwith low
insolation and a great diversity of potential predators. The response of the
Heliconius, which like most nymphalidbutterflies are dorsal baskers that
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102 TURNER
Figure1 Interlockingof the adaptationsof Heliconius

andtheir associatedplants in the,
tropical American
rain forests. Arrows
indicatecausalrelations, in mostcasesvia natural
selection.
absorb solar heat by means of their outspread wings (113), has been
increase of black markingsat the expense of other colors (36). This process
has been repeated by the distasteful North Americancheckerspot, Euphy-
dryas phaeton, which with its brilliant red and yellow spots on a black
ground looks very like a Heliconius (11, 101) and is also a dorsal basket.
The greater elongation of heliconiine wings (which allows more etiicienlt
gliding) and the ability to fly using conventional flight [whichmost butter.-
flies lack (44)] as well as a poweredupstroke, permit precise control o!r
hovering, climbing vertically, and even flying backwards. This gives the
butterflies a maneuverability used to approach both host plants and roosts,;
(below) as well as to thread the intricately laced creepers in secondgrowth.
However,despite the rapid escape flight they make possible, such flight
characteristics must also expose the heliconiines to a greater risk of preda-
tion. The distastefulness which, along with warning colors counters this
problem, is effective against birds (13, 15, 103) and lizards (12). This
~
tastefulness leads to extensive muellerian mimicry(mutual resemblance.
amongseveral distasteful species). Along with manyother warningly col-
ored insects, Heliconiususe the defense chemistry of their larval host plants
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DARWINIANEVOLUTION OF HELICONIUS 103
for their owndefense, both plant and butterfly containing cyanogenicgluco-

sides, but the relationship is not a simple one (73a). The original coloration
has been brightened by the addition of a yellow amino acid pigment,
confined to the more advanced groups (17, 26), and by a chemically still
unexplainedintensification of the orange to brilliant red.
In the open, Passiflora vines can form thick carpets of vegetation (e.g.
P. foetida in roadsides and ditches), but in the forest and in small patches
of second growth they occur at low densities and are widely spaced; as
anyonewhohas looked for them knows, they are hard to find. This problem
also confronts the butterflies, manyspecies of which have developed re-

stricted homeranges [etttilla, cydno, sara, hecale, rnelpomene,erato (41, 85,
98)] in which they can learn the location of the host plants, which are
valuable resources not only to ovipositing females but also to males in
search either of virgin females or, in the charitonia-erato species group, of
mature female pupae, with which they mate before eclosion (54). The
rudimentsof this behavior are seen in the homingof,4graulis butterflies to
the plant on which they grew up (31). The capacity of Heliconius for
learning landmarks and feeding sites is obvious to anyone who has kept
themin captivity; in the wild they can even learn to avoid the place at which
the researcher habitually nets them (71)[ They readily learn to associate
food with particular colors (91, 92).
However,passion vines have evolved a secondline of defense, extra-floral
nectaries. These attract ants that prey on heliconiine eggs, larvae, and
possibly pupae (9, 54, 115). They also encourage a high density of hyme-
nopteran egg parasites (56). The two-fold effect of the abundanceof ants
and parasites is to select for (a) rapid developmentof the heliconiines early
stages, which suffer high mortality (56, 116) comparedwith the warningly
colored and protected adults [larvae are eaten also by Hemiptera (71) and
in open country by Polistes wasps; pupae maybe eaten by mammals(103)];
and for (b) one or both of two types of egg-laying behaviour: laying large
rafts of eggs, which give rise to troops of gregarious larvae (presumably
protected by this habit), and laying on the fresh growth around the meri-
stems, wherethere are fewer ants, and particularly on the very tips of the
youngtendrils [or rarely even on neighboring nonhost plants (118)]. Larvae
are defended also by muellerian mimicry (24, 25, 97, 103) and pupae
silver spots, which, whenseen against the light, cause them to resemble an
emptypupal shell. Both larvae and pupae are protected by spines (perhaps
against lizards and rodents), the functional importance of which is shown
by convergenceamongthe unrelated gregarious species (juno, doris, aoede,
sara) in which the long spines on the head are lost or muchreduced. Such
long spines wouldtangle with the next caterpillar whenthe head is turned
to chewthe edgeof the leaf. In these species the headspines are functionally
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104 TURNER
replaced by long, forward-pointing spines on the mesothorax, which is not

turned during feeding.
Wenowsee the first set of interlocking adaptations. The growth of many
of the vines is slow. The larvae of manyheliconiine species, especially those
that live on the small, fragile vines of the subgenus Plectostemma, are:
solitary and aggressive, defending their easily depleted food by eating:
1-1eliconius eggs (1, 8); even in gregarious species larvae mayeat subse-
quently layed eggs (99) or chewawaytheir substrate. Anegg-laying female:
is thus severely restricted for oviposition sites at any one time but is con..
fronted with a sparse, reliable, slowly renewingresource in the form of new

unoccupiedmeristems. The selective pressure is for her to learn the posi..
tions of the plants and bide her time. Femalesdo in fact exhibit great care
in assessing such suitable sites, using their maneuverabilityto inspect them
with eyes, antennae, and forelegs, and avoiding those already occupied (56).
The anatomicalpeculiarities of Heliconius--the stilt legs, large head and
eyes, and long wings---can be seen as structural adaptations to this wayof
life (54). Someelaboration of the nervous system is expected, but although
muchis knownabout its physiology, including the regulation of behavior
by a circadian clock (93), this prediction has yet to be tested by comparison
with other butterflies.
Life History Strategies

The combinedeffect of selection for rapid early development [to escape
predation (99)] and prolongedadult life (to wait for the egg-layingsites)
produced a generation structure reversing that of most butterflies: Egg,
larva, and pupa last less than four weeks (sometimes considerably less,
varying with species and latitude), whereasadults have life expectancies of
months[ethilla, xanthocles, erato, charitonia (29, 41, 71, 98)] and even live
long enough to show senescence in the form of decreased survivorship
amongold butterflies (29).
Most Lepidoptera use nutrients taken by the larva to produce a supply
of eggs (ready to be laid just after eclosion) whichis progressively depleted
during the short adult life (67). In Heliconiusthe nutrients are instead taken
by the adult. Femalesare often unable to lay for several days after eclosion
(99). Their eggs mature at a slow, steady rate of one to ten per day during
their whole life span (39, 40). Nutrients for egg production include amino
acids from the pollen of Anguria flowers (Cucurbitaceae) and to a lesser
extent from supernumerary male spermatophores (10, 53). [In both these
features they are extendinga trend seen in other butterflies, first to econo-
mize on larval nutrients (by not weaving a cocoon) and second to take
nitrogenous compounds from amino acid rich nectars (2), bird drop-
pings (helieoniines and ithomiids), or other excrement (Phyciodes, Lerneni-
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tis, Apatura.] The Anguriaplants are, like the passion vines, inconspicuous
but persistent in the production of flowers at particular sites for monthson
end. Feeding on them, the butterflies regularly work learned trap-lines
within their homeranges (41, 54). They also exhibit the special behavior
needed to collect the pollen in a cake on the tongue and then digest it
externally (53). Heliconius are the chief pollinators of Anguria, which are
dioecious and show a markedly male-skewedsex ratio. (Male flowers are
presumablyselected for ever-increasing pollen production and females for
mimicry of the males.) The butterfly and the plant are thus locked in
mutualistic relationship which, by sustaining the butterflies at low but

constant population densities in the face of the long-te~n anti-herbivore
tactics of their larval host plants, maybe crucial to the continuanceof the
whole Passiflora-Heliconius-Anguria system (54).
Sociobiology
The modification of dourtship behavior into a ritual, elaborate but spatially
restricted whencomparedwith the long straight chase of the open country
Agraulis (32, 33, 96, 99), can also be seen as appropriate to a butterfly with
a learned homerange in a physically complexhabitat. (Observations on the
courtship of several species unfortunately remain unpublished.) Sexual se-
lection must have favored males who rememberedthe positions of host
plants and of mature female pupae. The resulting tendency to mate with
newly eclosed females has becomemodified, in the erato-charitonia group,
into mating with the pupa before eclosion (54).
Longevity, homeranges, and landmarklearning, generated and sustained
by the relation of the butterflies with the two plants, make possible the
formation of communalroosts (5, 32, 37, 65, 98, 102, 120) to which the
butterflies homerepeatedly, though not with absolute regularity (65, 98,
119), at night. In Heliconius (Heliconius) roosts are usually on dried creep-
ers hanging from branches, an excellent protection against night crawlers.
In short-lived butterflies lacking a learned territory, such roosts could only
be formed with the help of pheromones.
The small size of the breeding populations, restricted homeranges, and
broadly overlapping generations, allowing a butterfly to fly with several
generations of its descendants, are expected to lead to moderately high
levels of kinship within populations and hence to the evolution of cooper-
ative and altruistic behavior through kin selection (4, 99). The communal
roosts, which involve visual signalling between the butterflies (J. L. B.
Mallett & D. A. Jackson, unpublished), presumably give added protection
by aggregating individuals within the homeranges of a small number of
educable predators compared with the number that would require educa-
tion if the butterflies were dispersed. Such roosting populations maybe
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106 TURNER
nothing morethan selfish herds (63), as maygregariouslarvae. Thefemales

of four of the specieswithgregariouslarvae (D. juno, I-I. dorisz, tt. xantho-
cles, I-I. sara)cooperatein jointly laying batchesof eggs(71, 99). This may
be largely selfish behavioraimedat increasingthe size of the larval troop
abovethat producedby a single female (given the unusual ovarian physi-
ologyof tteliconius). In the last twospecies, whichlay on meristems,it may
alternatively be altruistic or cooperativebehaviorin whicha limited re-
source is shared with a relative. Either way, this behavior, and communal
roostingitself, will evolvemorereadily whenthe action benefits kin as well
as self. It is possible that the communal roosts allow the most highly
developedsocial behaviorof all, the cultural transmissionof information:
Youngbutterflies maylearn the location of host and pollen plants by
followingan older relative fromthe roost (56).
Theuse of an olfactory chastity belt, a pheromone the maleplaces on the
femaleat mating(55), is probablynot, as first appears,cooperativebehavior.
The pheromoneis advantageousto the female (whoshould not waste time
on unnecessary matings) and to the first male (whoshould protect his
spermatophore),but the subsequentmaleswhoare repelled by it are proba-
bly not so muchcooperating--i.e, observing a gentlemensagreementnot
to molest a girl whowears a weddingring--as they are saving the time:,
energy, and wingdamageinvolved in courting an unwilling female.
As Fisher suggested, the evolution of warningcolor and distastefulness
in the groupmayhavebeenproduced,or at least enhanced,by kin selection,
for the individualsacrificed in educatinga predatorbenefits not itself but
its conspccifics(4, 98, 99). However, the distastefulnessof the wingsmakes
individualselection possibleas well, by causingan individualto be released
relatively unharmed (12). Enhancement of distastefulness of courseties the
adaptationwebtogether: Byincreasingadult longevity,it contributesto the
unusual overlap of generations, to host-plant finding, and to communal
roosting (Figure 1).
EVOLUTION, HISTORY, AND GENETICS

The Panglossian Paradigm?
Acritic could object that, evenwith the corroborativedetails omittedfor
lack of space, the aboveis simplyanotherapplicationof the adaptationist
programor a sequenceof just so stories; an interpretation of the ecology
of Heliconius in Darwinianterms, not a test of neoDarwinism. Howdo we
knowthat someof the features observeddo not serve other, undiscovered
2This multiple parentage accounts for the contradictory genetic results obtained from
batches of doris eggs found in the wild (ef 28, 82).
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functions (70).9 Canwe be certain they are not merelythe spaces left over
betweenother adaptations (60)? All is perhaps not yet for the best in this
world: Agraulis in California, where both they and their food plants have
lived for less than a century, prefer to oviposit on a Passiflora that does not
produce optimumgrowth and survival of their larvae (30, 31).
Of course, one sound reason for accepting a theory like neoDarwinism
is its great power of explanation and prediction when applied to such
intricate ecological systems as this one, but to meet this justified challenge
we must examine an adaptation simple enough to be of unambiguousfunc-
tion, and capable of being analyzedgenetically. Mimicryfulfills these crite-

ria.
Mimicry and Adaptive Radiation

There is extensive general evidenee for the effectiveness of mimicry(107).
Both the distastefulness and the ability of mutually mimetieHeliconius to
deceive birds have been shownexperimentally (15). Within Heliconius there
has been extensive divergence of color pattern within species groups, ac-
companiedby markedconvergence amongspecies in different groups; this
produces a pattern of mimicrytings that cuts right across the taxonomic
groups or, if one likes, produces parallel series of related species, each
species group exhibiting most of the knowncolor patterns (104) [taxonomic
details and illustrations in (23)]. This miniature exampleof standard adap-
tive radiation and convergence is exceptional in that we can analyze its
genetic basis by meansof crosses within single species. For the beginning
of the process can be seen betweengeographical races within certain species.
tt. melpomeneand erato, for example, exhibit a series of parallel raees
(great divergence within each species, with almost perfect one-for-one mim-
icry betweenthemin a given area--Figure 2) analogousto the parallel series
of species at a higher taxonomiclevel. If the races of melporneneand erato
were to speciate, they wouldin fact produce just such a series of parallel
species.
It is widely believed that the lowland rain forests of South America,far
from having a long history of stability, becamemuchreduced during cool
dry periods that coincided with the glaciations on higher ground and at
higher latitudes (84; extensive reviews in 80). Climatic deterioration split
the forest into island refuges separated by grasslands, and generated raee
or species formation in forest birds (61), lizards (112), trees (79),
butterflies (27). The ithomiine butterflies were the first organismsfor which
this system was proposed (48). There is a good correlation between centers
of endemismfor butterflies, birds, lizards, and trees, and the position of
refuges determined from paleoecologieal evidence (21, 22).
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108 TURNER
6
10
1 2 3 4 7 8 1 2 3 4 5 6 7 8
Figure 2 Parallel variation, distribution, and phylogeny of Heliconius melpomene(left) and

fteliconiu~ erato (right). Simplified from (83, 110). Numbersdenote existing forms; letters,
hypothetical ancestors. For color illustration, see (99, 101).
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A Model for the Evolution of Mimicry
This historical reconstruction, accompaniedby our knowledgeof mimicry

and of the genetics of melpomeneand erato, allows us to examinethe claim
(89) that evolution in the South Americanforest refuges is evidence in favor
of the punetuational modelof evolution. This model holds that evolution
occurs mostly in rapid bursts, associated with catastrophic speciation (phy-
letic splitting) in small isolated populations, separated by long periods of
evolutionary stasis. However,in melpomeneand erato isolation from gene
flow is unlikely to be the cause of the really remarkableracial divergence

within each species. First, gene flow even in continuous forest is much
restricted by the butterflies restricted homeranges (41, 106). Second, the
cornerstone of warningcolor is the presentation to the predator of a signal
identical to one that it associates with somethingnasty. Muellerian mimics
will be subject to rather strong normalizing selection as predators sample
deviant individuals on the chance that they maybe palatable, a prediction
confirmedexperimentally by the increased rate of predation (higher mortal-
ity plus greater beak damage)on Central Americanerato with artificially
altered patterns (5). The racial divergence shownin Figure 2 has occurred
in the face of this normalizing selection, and isolation from gene flow can
hardly have made muchdifference.
The paradox can be resolved through the Fisher-Nicholson two-stage
model for the evolution of mimicry (47, 75, review in 107). Muellerian
mimicryarises because predators generalize--i.e. avoid patterns that re-
semble,but are not identical to, the learned warningpattern. If two distaste-
ful species are sufficiently similar to be mistakensometimesfor one another,
then those extreme individuals in each species that more closely resemble
the other will receive greater protection. Thusthe two species will be subject
to directional selection towardsomeaverage of their two patterns; given the
appropriate genetic variation, they will slowly becomerather accurate
muellerian mimics. If a number of species are involved, then a mimicry
ring will be formed (83). However,generalization by predators declines
with decreasing resemblanceof the signals (38), until it must becomenegli-
gible. Thus if two patterns are very different, predators never mistake one
for the other. As two such patterns cannot converge, several stable mimicry
rings can persist in the samehabitat, although at first thought one expects
them all to converge to a single warning pattern (83). This explains the
paradox that two distinct patterns of bumblebee coexist in Europe(78) and
no less than five mimicryrings of distasteful butterflies within the South
Americanrain forests (77).
However,suppose that one species is muchbetter protected than another
by being either more unpleasant or more numerous(greater numbers give
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110 TURNER
greater protection for the same reason that minority deviants are selected.
out). In this case, any mutationin the less-protected species that sufficiently
resembles the better protected will be at a selective advantage and will.
spread; in this waytwo very different species can becomemimicsby conver-.
gence of the less protected toward the more-protected, just as happenswitl~
a batesian (palatable) mimic (81) (Figure 3). This convergence will
only if the patterns are similar enoughto be bridged by a single mutation,
a fact beautifully illustrated by the relict species/t, hermathena,one popu.-
lation of which mimics//, erato by means of a single mutation that wipe,;
out most of its yellow marks in an area where it differs from erato only by
those marks. In other populations it flies with races of erato from whichit
differs so extensively in color and pattern that several mutations wouldbe
required, and these it does not mimic (25). The mutation, it is important
to note, does not have to produce perfect mimicry, but only mimicry that
is accurate enough to provide an advantage over its original allele (the
accuracy required decreasing as the difference in protection betweenthe two
species increases). Oncethis first phase (the spread of a newmutation)
largely completed, then the two species, which nowresemble each other
fairly closely, will be subjected to selection for the gradual convergencethat
will render the mimicry even more accurate. Thus in this second phase,
modifier genes affecting the expression of the initial major mutation witl
becomeestablished in the population (83).
Wehave therefore proposed (83) that the racial divergence within melpo-
mene and erato has been produced by differences in the abundance (or
degree of protection) of different mimicryrings in different refuges, with the
species comingto mimic whichever abundant, protected species was within
reach by a single mutation (probably in most cases ithomiine and pierine
butterflies). In accord with this, our extensive genetic experiments show
that the races differ by a limited numberof mutations of comparativelylarge
effect (Table 1). In accord with the two-phasetheory, there are also consid-
erable minor gene differences affecting the expression of the major genes,
and even their dominance and epistatic relations. Although major muta-
A B PATTERN x A Y B PATTERN
Figure3 Distributionof pattern phenotypes (shaded)on an arbitrary linear scale in two

distastefulspecies.Heavy
lines representfitness(in freedomfrompredation).Onthe left, the
twospeciesare selectedfor gradualmutualconvergence; onthe right, speciesB will converge
to speciesAonlyff it produces a mutation witha patternin the regionxy. From(83, 110).
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tions are involved, mimicryhas not arisen, perfect fromthe start, by means
of a hopeful monster.
It has been pointed out that evolution of this kind does not necessarily
require isolation in refuges. Changesin butterfly abundance within a contin-
uous forest could also provokethe capture of different populationsof a
species by different mimicryrings, and hence the parapatric formationof
races (7, 45, 114). As the selective processes involved in allopatdc and
parapatricrace formationare the same,the questionis really one of history:
Did the races of melpomene anderato mostly arise in isolated refuges (109)?
In addition to the biogeographicalevidence in favor of the allopatric model

(22), there are reasons for believing that races of this kind will formmore
Table 1 Genes controlling pattern differences in two species of Heliconius
H. melpomene
Race: (1) a (2) (3) (4) (7) (8) Function of gene
+b O O O + + Red fw base
O O + + + Red hw rays
0 + + + O O Red fw band
0 + + + O O Yellow fw band
0 O O O O + Yellow hw bar
+ + O + + O Fw cell spot
0 + + O O O Red/orange
0 O O O + O Broken fw band
0 + + + + + Red color responds
0 + + + + + Split fw band
+ O O O O O Fw triangle
+ O O O O O White fw band
H. erato
Race: (1) (2) (3) (4) (5) (6) Function of gene
+ O O O O + + + Red fw base
+ O O + O + + + Red hw rays
O + + + + O O O Yellow fw band
O O O O O O O + Yellow hw bar
O + + + + + + + Split fw band
+ + O + + + + + Shortened fw band
+ O O O + + + + Broken fw band
O O O O O O O + Hwrectangles
O O O O O O O Yellow hw bar
O + + O O O O O Red/orange
+ O O O O O O O Band responds
+ O O O O O O O White fw band
O + + + + + + + Round fw band
aNumber code for races refers to Figure 2.
b+ = recessive allele, O = dominantallele, fw = forewing, hw = hindwing. From(82, 83,
100).
Annual Reviews
112 TURNER
often in refugesthanin continuousforest, for the flora andfaunain a refuge,

like thoseonanyisland, are subjectto progressiveextinctionof species(16).
Asa result, refugescometo differ in a rather haphazardwayin their species
composition.This will ensure, evenif noneof the distasteful butterflies
becomes extinct, that they will differ in abundancebecauseof the extinction
of competitors,parasites, host plants, competitorsof host plants, andso on
(106). AsHeliconiuspopulationsare small, the appearanceof a newmuta-
tion maybe delayed for a considerable time, and hence the longer these
changesin abundancelast, the morelikely they are to generatenewmimetic
patterns. For example,somepopulationsof herraathena(above) that could

mimicerato by loss of the yellowbars do not do so; probablythe appropri-
ate mutation has not yet occurred in them(25). Changesin abundance
a continuousbiomeare temporary;those in a refuge are permanent,until
the refuge expandsagain (106, 109); such refuges must have lasted for
several thousandyears in the Quaternary(64). Thehypothesisis therefore
that populations of melpomeneand erato have switched mimicryrings,
usually whenconfined in forest refuges during the Quaternary.Theraces
so evolved have nowspread out, meeting and producing hybrid zones at
their boundaries,whichare stabilized by disruptive selection against the
minorityof hybridbutterflies (83, 103).
Gene Substitutions or Punctuation?
Themodeljust described can be applied to the general problemof evolu-
tionary novelty. Noveladaptations mayarise in remainingspecies whenan
ecologicalnicheis emptiedby the extinction of the species occupyingit. A
mutationin any of the other species giving adequate adaptation to that
nichecan then find itself at an advantage,as it escapesfromintraspecific
competitionin its old nicheandis no longersubjectto interspecific competi-
tion with a muchbetter adapted form in the newniche. Just as with
mimicry,the adaptation need not be perfect fromthe start, but is often
likely to involve a majormutation. Alterations like that observedin the
articulation of snakemandibles(49) can readily be explainedby this model.
Asniches mustbe vacatedrather rarely, evolutionin interveningperiods
wouldconsist largely of the speciesdiggingitself deeperinto its established
ecological niche. Theevolutionary conservatismso producedis shownby
the resistance successfully offered to the evolution of mimicryby sexual
selection and the other functions of butterfly colors (107, 108). Have
therefore arrived at an explanationof the punctuationalmodelof evolution?
Wecan answerthis from our genetic data (Table 1) (83).
Thetheoremcalled Haldanessieve (62, 72) states that dominantalleles
are substituted under natural selection muchmorerapidly than recessive
ones. A hypothetical pattern producedentirely by the knownrecessive
Annual Reviews
alleles would thus closely resemble the ancestral pattern of a Heliconius

species. Both for melpomeneand erato this is a black butterfly with yellow
bars (Figure 2). This suggests that the mimicry of the races of the two
species results from.parallel evolution (muchmore likely than the alterna-
tive, that the paired races have all convergedon one another from disparate
ancestors). Sucha reconstruction is supported by the fact that the nonmi-
metic (and hence perhaps slowly evolving) relatives of both species have
similar yellow and black pattern (83).
As the sieve theorem tells us that recessive alleles are ancestral and
dominantalleles derived, we can readily use the genetic data (Table 1)

estimate the phylogenyof the races by the weighted invariant step method
(46). Of several minimum-length trees obtained (110), the ones selected
illustration (Figure 2) are the most plausible in terms of the geographical
distribution of the races, which also produceancestral patterns at the nodes
that are still shownby relict, nonmimetieraces of other species. However,
the detailed accuracy of the cladograms is unimportant. Any plausible
cladogramof the races would, like those shown, have a rather small number
of major gene substitutions in each branch (cross bars in Figure 2). If
makethe reasonable guesses that the trees span at least 30,000 years [the
last glacial cycle (64)] and that selection coe$cients were at least 1%then
the patterns would have been constant for long periods, punctuated by
bursts of rapid change lasting less than 400 years (less than 4000 genera-
tions from the time whenone butterfly in a thousand had the new pattern
to that whenone in a thousand had the old.) To judge from early illustra-
tions there has not been muchchange since the eighteenth century (95). But
this sequencediffers from punctuationai evolution as it is usually described
(43, 68, 89) in that (a) it is not associated with speciation in small isolated
populations that then replace their ancestor, (b) the rapid changes are not
necessarily associated with the branching of the tree (that is howwe detect
them in the present case, but a species represented by a single population
could clearly undergo the same changes with no branching), and (c)
genetic work shows that no hopeful monsters are involved. Far from the
changes being abrupt alterations in the species, they look remarkably like
gene substitutions as conventionally understood in neoDarwiniantheory.
At the molecular level the butterflies showevery sign of undergoing slow,
gradual divergence alongside the morejerky evolution of the color patterns
(111). If the formation of races in rnelpornene and erato has taken only
twenty to thirty thousand years, then even allowing for loci controlling
color pattern that mayhave remained invariant during this time, the rate
of evolution of the patterns is considerably faster than that observed in
proteins (74, 109). The evolution of color patterns and enzymesoccurs
different modesand perhaps at different speeds.
Annual Reviews
114 TURNER
BRANCHING
Race Formation and Speciation
Wetend to think of speciation as the preludeto adaptiveradiation, whether
gradual or punctuated(69, 89). In I-leliconius, however,a significant
amountof adaptive radiation occurs before speciation, and there is every
reasonto believe that the genetic changesin color pattern betweenspecies
are of the sametype as the genetic changesbetweenraces, and indeed as
the mutations that appear in captive populations. The pattern of mel-
pomenesclose but superficially very divergent relative H. ethilla can be

constructed almost entirely from pattern elements controlled by genes
knownin melpomene(110), and combinations of certain genes in erato
producea pattern close to that of its relative/t, telesiphe(83). Rarecolor-
changemutantsare knownin several species, and have been investigated
in melpomene (P. Braketield, unpublished). It is evenpossible that some
speciation occursmorerapidly than somerace formation(a possibility that
wetend not to considerbecauseof our belief that evolutioncorrelates witli
the taxonomichierarchy). Someclosely related species could branchfrom
a cladogramlike Figure 2 rather high up amongthe diverging races!
The Insect-Plant Arms Race
Theddicate relations between1-1eliconiusandPassifloralead to regulation
of the demographyof the butterflies by the plants. In Costa Rica the
abundanceof the different species correlates with the abundanceof the
meristemsof their host species; whenplotted betweendifferent sites, the
numberof I-leliconius species correlates with the numberof Passiflor~
species in the habitat (59). Becausethe numberof coexisting Passiflor~.
species is limited (to a dozen,for unknown reasons), the numberof coexist..
ing 1-1eliconiusis likewiselimited. Thenumber of butterfly speciesis greater
than that of Passiflora becausethe larvae of someheliconiines can coexist
by feeding on leaves of different ages (6, 8). Therare monophagous/-.
nattereri is threatenedwith exinetionas its oligophagousrelatives invade
and out-competeit on its host plant (18). Thebutterflies partition the
habitat spatially as well. Co-mimics feed on different host plants, yet fly
together, but fly in different places (e.g. openareas as against the shadeof
the trees) fromtheir closest phyletic relatives (85, 117). This observation
raises an interesting question: Doesthe mimicrydeterminethe habitat
choice, or do butterflies that have the samehabitat cometo mimicone
another?[Perhaps the mostspectacular spatial difference is betweenthe
nonmimetichigh-flying males and the mimeticdeep-forest females of
nattereri (18).] Suchspatial correlation mayhaveevolvedin several ways:
(a) Predators maysimilarly divide the habitat; (b) predators mayidentify
a butterflypartly on the basis of the placein whichit flies, or (c) the opticM
Annual Reviews
properties of the butterflies patterns mayin someway be adapted to the

visual mosaic presented by the habitat (77).
Experiments with Central Americanheliconiines showed that host-plant
specificity can be nutritional (as in erato, whichgrowsbetter on its preferred
hos0 or purely behavioral (as in melpomene,which lays on P. oerstedii but
grows just as well as its muchmore catholic relative H. cydno on a range
of host plants) (86). Agraulis in California refrain from laying on Passiflora
species that are nutritionally suited to their larvae (31). It is not known
these cases whether (a) the butterfly has evolved an avoidance of a plant
that is unsuitable for ecological reasons (e.g. high larval mortality inflicted
by competitors), or (b) the butterfly has not yet evolved the ability
respond to a suitable host, or () the plants have escaped the attentions
the butterfly by ceasing to produce the compoundsthat stimulate oviposi-
tion. In the subtropical parts of Brasil, the Heliconius species are muchless
restricted in their choice of plants, possibly because there is little inter-
specific competition during the seasonal surge of growth of Pass(flora (6).
The effects of the limitation placed on Heliconius diversity by competitive
exclusion and biochemical restriction on their host plants exert long-term
control on the evolutionary radiation of the butterflies: The correlation
between the taxonomic subgroups of the butterflies and the plants [Table
3 in (23)] can easily be interpreted as indicating the adaptive radiation
groups of butterflies from ancestors adapted to the plant defenses of the
ancestral species of the groups of Passifiora (8). This is a microcosmic
confirmation of the general herbivore-plant coevolution hypothesis (42).
It wouldbe amusingto think of this as an interlocked systemlike the one
in Figure 1, with the butterflies driving the adaptive radiation of the plants.
The additional defenses against Heliconius, which have all been moreor less
cracked by one or more Heliconius species, show that the butterflies and
plants are locked in an evolutionary arms race (35). Such defenses include
(52, 54, 56-58) bizarre diversification of leaf shape(to avoid shape-recogni-
tion by ovipositing females); leaf mimicryOf other plants; trichomes that
catch and bleed younglarvae to death; mimicsof butterfly eggs that deter
the females of solitary species; deciduous leaves and fake tendrils that
jettison eggs and larvae (58) (M. C. Singer, unpublished); and additional
toxic chemicals (P serratifolia can poison/t, isabella larvae). However,
adaptation does not necessarily involve cladogenic speciation. Therefore it
does not necessarily follow that the diversification (as distinct from evolu-
tion) of the Passiflora is being generated by the butterflies.
Ecological Change and Speciation

But this does suggest a modelfor speciation in Heliconius, one of the major
uninvestigated areas in the biology of the group. Althoughthe plant in an
Annual Reviews
116 TURNER
evolutionary race will alwaystend to produce gradually developeddefense,,;

against the herbivore, matched gradual changes in the herbivore should
normally be able to counter them. Only a rather large mutational change
in the plant (e.g. one that blocks the synthesis of an oviposition stimulant)
that requires a similarly large counteracting mutation in the herbivore is
likely to allow the plant to escape, at least temporarily, fromthe herbivores
attentions. (This is fully analogous to the waiting time required for the
evolution of muellerian mimicry.) But the spread of a successful counter.-
mutationin one of the butterflies will result in a significant wideningof it,,;
ecological niche (and of course an increase in abundance, which mayinduce

other species to mimicit). Shifts in host-plant preference will also occur in
refuge populations as a result of changes in abundance, and as a result of
actual extinction of Passiflora species. Further, a changeof habitat, result.-
ing from the adoption of a new mimeticpattern (if this indeed occurs) will
itself tend to select for a changeof host plants, since the array of Passiflor, t
species visible to the females will be changed.
Speciation rather than fusion of two races may then perhaps occur when
a large shift in host-plant preference, allowing coexistence (hence mutual
invasion of range), is added to significant changes in color pattern. The
disruptive selection inflicted by predators on the minority hybrid patterns
will encourage pre-mating isolation. Becausecolor is an important recogni-
tion signal during Heliconius courtship (32), the changedmimetic pattern~
themselves might provide the isolating mechanism.In this way, moderately
large genetic and ecological changes wouldaccompanyspeciation, as in the
punctuational model; but in contrast to somepresentations of that model
[e.g. in (68)], speciation is simply an outcomeof race formation, not
independent process.
CONCLUSION
Speculation aside, the hard evidence of our genetic experiments showsthat

evolutionary novelties can arise by major gene mutations, permitting adap-
tation to a newecological niche. Becausethe emptyingof niches (or filling
of mimicryrings) tends to occur by extinction on islands, this process may
be (but is not necessarily) accompaniedby cladogenic speciation. No hope-
ful monsters are needed! Mutation alone can produce an adaptation to a
newniche that, in spite of initial imperfections, is fitter than the established
adaptation to the old; the new adaptation is then refined by the selection
of modifier genes. The comparative scarcity of such major mutations, and
of emptied niches, could account for muchof the conservatism (stasis)
evolution. There is no significant difference betweenold-fashioned ongoing
neoDarwinian evolution [the substitution of new dominant mutations by
Annual Reviews
DARWINIAN EVOLUTION OF HELICONIUS 117
natural selection is one of the best-attested facts of experimental population

genetics (66)] and newfangled on-and-off-going punetuational evolution.
Insofar as it is correct, the new theory is simply the old theory dressed in
new terminology.
ACKNOWLEDGMENTS
To Woodruff Benson, Keith Brown, Roy Davis, Charles Ellington, Law-

rence Gilbert, James Mallett, and the late Philip Sheppard, I am most
grateful for the continued exchange of ideas and information that has made
this review possible.
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Adaptation and Evolution in Heliconius. A Defense of NeoDarwinism

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Adaptation and Evolution in Heliconius. A Defense of NeoDarwinism

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Annual Reviews

AnnRez EcoLSyst 1981. 12:99-121

ADAPTATION AND ~4189

EVOLUTION AND NOVELTY

madly the question whether the synthetic theory of population genetics,

COEVOLUTION AND ECOLOGY

G. E. Hutchinsons bon mot "the ecological theatre and the evolutionary

Special Adaptations in Heliconius

DARWINIANEVOLUTIONOF HELICONIUS 101

The forest-dwelling Heliconius (subgenus Heliconius) are predominantly

Figure1 Interlockingof the adaptationsof Heliconius

DARWINIANEVOLUTION OF HELICONIUS 103

for their owndefense, both plant and butterfly containing cyanogenicgluco-

also confronts the butterflies, manyspecies of which have developed re-

replaced by long, forward-pointing spines on the mesothorax, which is not

fronted with a sparse, reliable, slowly renewingresource in the form of new

Life History Strategies

DARWINIANEVOLUTIONOF HELICONIUS 105

mutualistic relationship which, by sustaining the butterflies at low but

nothing morethan selfish herds (63), as maygregariouslarvae. Thefemales

EVOLUTION, HISTORY, AND GENETICS

DARWINIANEVOLUTION OF HELICONIUS 107

tion, and capable of being analyzedgenetically. Mimicryfulfills these crite-

Mimicry and Adaptive Radiation

Figure 2 Parallel variation, distribution, and phylogeny of Heliconius melpomene(left) and

DARWINIANEVOLUTION OF HELICONIUS 109

A Model for the Evolution of Mimicry

This historical reconstruction, accompaniedby our knowledgeof mimicry

flow is unlikely to be the cause of the really remarkableracial divergence

Figure3 Distributionof pattern phenotypes (shaded)on an arbitrary linear scale in two

DARWINIANEVOLUTIONOF HELICONIUS 111

In addition to the biogeographicalevidence in favor of the allopatric model

Table 1 Genes controlling pattern differences in two species of Heliconius

often in refugesthanin continuousforest, for the flora andfaunain a refuge,

patterns. For example,somepopulationsof herraathena(above) that could

DARWINIANEVOLUTION OF HELICONIUS 113

alleles would thus closely resemble the ancestral pattern of a Heliconius

dominantalleles derived, we can readily use the genetic data (Table 1)

pomenesclose but superficially very divergent relative H. ethilla can be

DARWINIANEVOLUTION OF HELICONIUS 115

properties of the butterflies patterns mayin someway be adapted to the

Ecological Change and Speciation

evolutionary race will alwaystend to produce gradually developeddefense,,;

ecological niche (and of course an increase in abundance, which mayinduce

Speculation aside, the hard evidence of our genetic experiments showsthat

DARWINIAN EVOLUTION OF HELICONIUS 117

natural selection is one of the best-attested facts of experimental population

To Woodruff Benson, Keith Brown, Roy Davis, Charles Ellington, Law-

this review possible.

tteliconius and related genera. Ant~

DARWINIAN EVOLUTION OF HELICONIUS 119

49. Frazetta, T. H. 1975. ComplexAdapta- Part I. Trans. CambridgePhilos. Soc.

bee color patterns: a mimeticinterpreta- 95. Turner, J. R. G. 1967. Some early

the geography, genetics, and taxonomy 98. Turner, J. R. G. 1971. Experiments on

DARWINIAN EVOLUTION OF HELICONIUS 121

in the Emergenceof the Biosphere, ed. Dryas butterflies (Lepidoptera: Nym-

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