Chapter 1 - Introduction
Introduction
This thesis concerns the speciation process in a pair of tropical butterflies;
Heliconius melpomene and H. cydno.
In this chapter, speciation theory and the study organisms will be introduced.
Chapter 2 summarises the literature on introgressive hybridisation in animal taxa, its
consequences and possible implications. Chapters 3 and 4 present gene genealogies
which provide evidence for selective gene flow between the species. These chapters
also help to clarify phylogenetic relationships in the genus. Chapter 5 describes
experiments performed to test the hypothesis that F1 hybrids will be preferentially
taken by avian predators. In Chapter 6, conclusions are drawn regarding how this
thesis has contributed to current knowledge on genealogy and speciation in H.
melpomene and H. cydno. Appendix 1 is a paper senior authored by Margarita
Beltrán, but to which I contributed. This paper describes gene genealogies of
heliconiine butterflies (from the genera Heliconius, Laparus, Eueides, Dryadula,
and Dryas), based on mtDNA and nuclear genes.
Speciation
Species and their formation are of major importance for many fields of biology such
as ecology, conservation, taxonomy and evolutionary genetics. Historically, species
were seen as separate units, created individually by some higher force, but this view
changed with the publication of Darwin’s “On the Origin of Species” (1859).
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Darwin’s theory that species evolved from one another was hotly contested initially,
but eventually became accepted. This led to an explosion of interest in studies of
speciation, defined as the process leading to the formation of a new species. This
began with the Modern Synthesis of Darwinian evolution and Mendelian genetics
(Dobzhansky, 1937). Over time, the popularity of speciation waned as new issues
were perceived to be more important (Barton, 2001). Recently, there has been
renewed interest in the subject. Furthermore studies have become more focused on
sympatric and parapatric, as opposed to allopatric speciation.
The most informative method for studying the process of speciation is to look at
intermediate cases where taxa still hybridise in the wild, but have developed some
degree of reproductive isolation. The majority of studies of hybridising taxa have
involved hybrid zones, where hybrids are present in large numbers (e.g. Endler,
1977; Barton and Hewitt; 1989; Harrison, 1993). Although these studies provide
much useful information, it could be argued that they teach us little about speciation,
as the taxa have not yet speciated (Jiggins et al, 1996; Jiggins and Mallet, 2000). A
better approach might be to investigate species that hybridise only rarely in the wild,
and show a greater degree of reproductive isolation.
Reproductive isolation
In order for speciation to occur, strong barriers must be present to prevent two
species from mating and forming viable offspring. Reproductive isolation is any
barrier that prevents successful reproduction between individuals, or reduces the
fitness of a hybrid once it is formed. If a group of individuals is reproductively
14
isolated, gene flow with the rest of the population is reduced and speciation thus
becomes possible. Isolating mechanisms or barriers can take many different forms,
but can be divided into two major categories: pre - and post-mating barriers.
Pre-mating isolation
Pre-mating or prezygotic isolation is the process whereby species are prevented
from forming hybrids by one or several barriers acting before fertilisation. These
barriers may be geographical, ecological, behavioural or morphological (Mayr,
1963).
Geographical isolation occurs when species are prevented from cross-mating due to
spatial separation, for example by a water body, mountain range, continental drift,
drying lakes or island formation (Dobzhansky, 1937; Mayr, 1963). Ecological
divergence can also drive speciation, examples being habitat divergence and
resource partitioning (e.g. Dobzhansky, 1937; Jiggins and Mallet, 2000; Schluter,
2001; Via, 2001). Behavioural differences can prevent species from mating
together, for example the species may exhibit different courtship rituals, colour
pattern or pheromones (e.g. Grant, 1993; Seehausen et al, 1997; Doi et al, 2001).
Morphological differences between species can provide another very strong barrier
to interspecific mating, e.g. physiological incompatibility of reproductive organs
(Sota and Vogler, 2001).
Pre-mating isolation will not be dealt with further here as it does not form a part of
this thesis.
15
Post-mating isolation
Post-mating or postzygotic isolation describes factors acting to reduce the fitness of
a hybrid zygote once it has formed. Post-mating isolation includes any form of
selection against hybrids, for instance hybrid sterility or inviability, environmental
selection, increased predation, or sexual selection against hybrids.
Genomic incompatibilities may cause hybrids to be inviable, or completely or
partially sterile (e.g. Arntzen and Wallis, 1991; Palopoli and Wu, 1994; Saetre et al,
1997; Coyne and Orr, 1998). Ecological factors may affect hybrids in that they may
not be as well adapted to their environment as the parental forms (e.g. Grant and
Grant, 1993); or they may show reduced mating success (e.g. Stratton and Uetz,
1986). There may also be increased predation on hybrids due to positive frequency
dependent selection. In this thesis, Chapter 5, I explore whether this is the case for
two Heliconius butterfly species.
Heliconius as a model system for studying speciation
Heliconius
Heliconius butterflies (Lepidoptera: Nymphalidae: Heliconiina) are a Neotropical
genus consisting of around 36 species. Ever since the work of Henry Walter Bates
and Fritz Müller, Heliconius butterflies have been important in studies of mimicry
and natural selection. Müller (1879) described a situation, now called Müllerian
mimicry, whereby an unpalatable species may evolve to mimic another unpalatable
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species, thereby gaining ‘safety in numbers’ against predators. Heliconius is a wellstudied group, and because of their bright coloration have been popular with
collectors. All species in the genus are warningly-colored and unpalatable, many
forming part of mimicry rings. They gain their toxicity from cyanogens, both from
ingestion of Passiflora at the larval stage, and synthesised themselves (Engler et al,
2000). Much is already known about their biology, genetics and ecology. Their use
of Passiflora host plants and pollen resources has been well documented (e.g.
Benson et al, 1975; Gilbert, 1975; Smiley 1978a, 1978b; Mallet and Gilbert, 1995;
Estrada and Jiggins, 2002). Other studies have looked at phylogenetics (see
‘phylogenetics of Heliconius’ section, this chapter); biogeography, (Brown, 1979),
coevolution with plants (Gilbert, 1975) and colour pattern genetics (Sheppard et al,
1985; Mallet, 1989; Jiggins and McMillan, 1997; Linares, 1997; Gilbert, 2003).
Heliconius are therefore ideal candidates for studies of speciation as they are well
studied, widespread and hybridise naturally in the wild (Mallet et al, 2002). Here I
investigate two separate, but related topics relevant to speciation between H.
melpomene and H. cydno. Firstly, I use gene genealogies to look for evidence of
introgression between the species, and secondly, I describe experiments designed to
test whether F1 hybrids between the species undergo preferential predation.
Mimicry and predation
Aposematic coloration acts as a very strong predator deterrent in many taxa
(Guilford, 1990). There are three main schools of thought on how warning colour
may have arisen, driven by individual selection, kin selection and synergistic
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selection (Servedio, 2000). Individual selection works on the basis that any
individual has a chance of surviving a predatory attack, and will benefit if that
predator learns that it is unpalatable and so avoids it in the future (Järvi et al,
1981a,b; Wiklund and Järvi, 1982; Sillén-Tullberg, 1985; Tullrot, 1994). Kin
selection states that relatives of an aposematic individual may benefit from predator
protection by possessing the same mutation for conspicuousness (Fisher, 1930;
Waldman and Adler, 1979; Turner, 1984; Leimar et al, 1986; Tullrot, 1994). The
third theory of warning colour evolution is that of synergistic, or ‘green beard’
selection (after Dawkins “green beard genes” 1976). This theory works on the basis
that individuals will gain protection by having phenotypic and not necessarily
genetic similarity to other aposematic prey (Guilford, 1985, 1988, 1990).
Heliconius species are aposematically coloured Müllerian mimics, and gain
protection against predators by mimicking other unpalatable species. This can be
seen as a form of synergistic selection.
Frequency dependent selection was first recognised by Poulton, (1890). There are
two types of frequency dependent selection, positive and negative. Negative, or
diversifying frequency dependent selection causes selection to be greatest on the
commonest colour pattern. This form of selection has been implicated in
maintaining colour pattern polymorphism (Haldane, 1955; Allen and Clarke, 1984;
Allen, 1988). Positive, or purifying frequency dependent selection theory dictates
that rare prey should be preferentially selected compared with commoner forms
when found alongside each other, and may be responsible for keeping hybrid
numbers low.
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Direct observation of predation in the wild would be the best method of assessing
whether a given butterfly taxon is preferentially taken over another, but this has
been found to be virtually impossible to achieve. In one study using the butterfly
species Vanessa atalanta, in 8000 days of observation spanning 22 years, only once
was predation by a bird seen (Swanson and Monge-Najera, 2000). To overcome this
problem, initial butterfly predation studies used artificial experimental set-ups, for
instance using coloured pastry baits with varying levels of toxicity to test whether
birds could learn to associate colour with taste, and to assess the importance of
frequency on selection (e.g. Turner, 1961; Allen and Clarke, 1968; Coppinger, 1969;
Brower, 1984; Greenwood et al, 1989; Weale et al, 2000). Many experiments use
computer simulations or mathematical models to test which prey a predator would
prefer (e.g. Turner et al, 1984; Schlenoff, 1985; Speed, 1999; Servedio, 2000; Bond
and Kamil, 2002). Other studies have used real organisms, but in an unnatural
setting, with dead prey items presented so that predators could choose between them
(e.g. Brower et al, 1963). Some studies used beakmarks found on butterfly wings as
an indirect measure of predation levels (Bowers et al, 1985; Pinheiro, 1997). Others
used caged wild birds and live prey (Chai, 1986, 1988, 1996; Ritland, 1998). Very
rarely have more natural situations been used to try to test theories of frequency
dependent selection on butterflies, including mark-recapture studies (Brower and
Brower, 1964; Benson, 1972; Mallet and Barton, 1989; Kapan, 2001), and releasing
insects at bird perches (Chai, 1986; Pinheiro, 1996; Pinheiro, 1997).
19
Although there has been a large body of work concentrating on butterfly predation,
most studies have concentrated on differences between species or colour morphs.
The only attempt to test differential predation on hybrids was performed in a hybrid
zone, using populations where the alternative form was absent (Mallet and Barton,
1989). In terms of speciation theory, we can learn relatively little from the results of
such experiments, as they do not involve colour patterns relevant in a speciation
context. Additionally, hybrid zones offer an unusual environment where hybrids are
often present in large numbers. Often, the home range of local predators may be
sufficient to have encountered colour forms from both sides of the hybrid zone, and
recapture rates may not accurately reflect the numbers of butterflies released. This
study did, however, show strong selection within species, suggesting that between
species, the effects may be even stronger.
A major gap in current knowledge about speciation in Heliconius is that of
frequency dependent selection on hybrids. Theory predicts that F1 hybrids between
aposematic taxa will be preferentially taken by predators, as they sport a novel
colour pattern not recognised as unpalatable. If this prediction is true, purifying
selection may play a great role in the process of speciation, as a strong post-mating
isolation barrier. In Chapter 5, I attempt to rectify this gap in our knowledge.
Phylogenetics of Heliconius
The genus Heliconius has undergone a rapid radiation, which may be due to
ecological adaptations, such as pollen feeding, traplining of food and oviposition
sites, and longevity of adults (Gilbert, 1975; Brown, 1981). The phylogenetics of
Heliconius species have been studied using wing-pattern alleles (Turner, 1981;
20
Sheppard et al 1985), morphological characters (Brown, 1981); and molecular data
(18s, 28s: Lee et al, 1992: and COI, COII and wingless: Brower, 1994, 1996a,b,
1997; Brower and Egan, 1997; Brower & DeSalle, 1998). The melpomene/cydno
group consisting of H. melpomene as the sister clade to the H. cydno group (H.
heurippa, H. pachinus and H. cydno) has been upheld in most studies to date (e.g.
Eltringham, 1916; Emsley, 1965; Brown, 1981; Brower, 1997). However, in Brower
(1996a, 1996b) the H. cydno group of species is found within H. melpomene,
rendering H. melpomene paraphyletic. A new study (Appendix 1) using mtDNA
(COI/COII) and nuclear genes (Tpi and Mpi) reveals a pattern concordant with
traditional studies at mtDNA loci, but shows a different pattern at Mpi and Tpi loci
(see chapter 3 and Beltrán et al, 2002 for more detail).
Heliconius melpomene and H. cydno
H. melpomene and H. cydno are recently diverged sister species (Brower 1996a;
Beltrán et al, 2002), broadly sympatric throughout their range in the Andes and
Central America. Both are unpalatable and warningly-colored, and differ markedly
in mimetic colour pattern. H. melpomene is typically red, black and yellow and
mimics H. erato, whereas H. cydno is typically blue-black and white or blue-black
and yellow (figure 1) and mimics species in the sapho/eleuchia group of Heliconius
(Linares, 1996, 1997).
21
Figure 1 – Heliconius melpomene, H. cydno, and their mimics. Left = French
Guiana races, centre and right = Panama races. Modified from Jiggins et al, 2001a.
The two species differ in larval and adult ecology (Smiley, 1978a,b; Mallet et al,
1998a; Naisbit, 2001; Estrada and Jiggins, 2002), and show habitat segregation
(Mallet et al, 1998a; Estrada and Jiggins, 2002). H. melpomene inhabits light second
growth forest and gaps caused by tree falls or rivers; whereas H. cydno prefers
dense, primary forest. However, there is considerable overlap and the two often fly
together. Jiggins et al (2001a) summarise speciation between these species and
show that pre- and post-mating isolation between them has resulted from an
adaptive shift in ecology and mimicry leading to pre-mating isolation. In association
with partial hybrid sterility, there has been subsequent evolution of assortative
mating between sympatric populations. For a summary diagram of factors
contributing to speciation between these species, see figure 2. There are around 29
described races, or colour morphs of H. melpomene, and 16 of H. cydno (Brown,
1979). The two species hybridise and backcross regularly in the wild (Mallet et al,
2002), although at a rate of less than 1/1000 (Mallet et al, 1998a). The number of
22
hybrids naturally occurring is kept low largely due to strong assortative mating
(Jiggins et al, 2001a).
23
Figure 2 - Factors contributing to speciation in H.melpomene and H.cydno
(proposed approximate order of events)
24
Introgression and phylogenetics
In H. melpomene and H. cydno, speciation is strictly not yet complete under the
biological species concept (Mayr, 1963), as hybrids are still found in the wild, albeit
at a very low rate. This makes these species ideal candidates for population genetic
studies looking for evidence of introgression. Heliconius butterflies are unpalatable
to predators, and have a diverse array of colour patterns that are typically mimetic of
other Heliconius species or of ithomiine butterflies. It is clear that most of these
patterns have evolved independently in separate lineages, using different
architecture, for instance, in the famous mimicry between H. erato and H.
melpomene (Turner, 1984; Sheppard et al, 1985). However, in some related species,
the same colour patterns occur again and again, with related races and species
apparently re-using the same genetic machinery to produce the same mimetic
pattern. These colour pattern/phylogeny anomalies appear especially frequently in
the melpomene/silvaniform Heliconius, a group in which most of the known wildcaught hybrids and backcrosses between species are found (Mallet et al, 1998a, b).
This suggests introgression is likely. H. melpomene and H. cydno typically belong to
completely different mimicry rings; however, several races of H. cydno in E.
Ecuador and E. Colombia (sometimes separated as the species H. tristero,
H.timareta and H. heurippa), appear to have adopted melpomene-like colour
patterns similar to those present in some races of melpomene. Another phylogenetic
anomaly is the adoption of melpomene-like colour patterns by H. elevatus, a
member of the silvaniform group, and only distantly related to the sister pair H.
melpomene and H. cydno. Its grouping with the silvaniforms is supported by
mtDNA as well as morphology (Brown, 1981; Brower and Egan, 1997; Beltrán et
al, 2002). Again, there is evidence for hybridisation and backcrossing between
25
melpomene and silvaniforms. Both phylogenetic anomalies suggest either
introgression being exploited as a source of ready-made adaptations (Gilbert, 2003),
or independent polyphyletic evolution of apparently homologous colour patterns.
Introgression between H. melpomene and H. cydno should theoretically be possible
as hybrids of both sexes are viable. Although female F1 hybrids are sterile in
accordance with Haldane’s Rule, male F1 hybrids are fertile and readily backcross
in both directions (Naisbit et al, 2001b).
In Chapters 3 and 4. I use gene genealogies to investigate whether there is evidence
for introgression between these two species.
26
References
Allen, J.A. (1988) Frequency dependent selection by predators. Phil. Trans. R. Soc.
Lond. B. 319: 485-503.
Allen, J.A. and Clarke, B.C. (1968) Evidence for apostatic selection by wild
passerines. Nature 220: 501-502.
Allen, J.A. and Clarke, B.C. (1984) Frequency dependent selection: homage to E.B.
Poulton. Biol. J. Linn. Soc. 23: 15-18.
Arntzen, J.W. and Wallis, G.P. (1991) Restricted gene flow in a moving hybrid zone
of the newts Tritarus cristatus and T.marmoratus in Western France
Evolution 45: 805-826.
Barton, N.H. (2001) Speciation. TREE 16(7): 325.
Barton, N.H. and Hewitt, G.M. (1989) Adaptation, speciation and hybrid zones.
Nature 341: 497-503.
Beltrán, M., Jiggins, C.D., Bull, V., Linares, M., Mallet, J., McMillan, W.O. and
Bermingham, E. (2002) Phylogenetic discordance at the species boundary:
Comparative gene genealogies among rapidly radiating Heliconius
butterflies. Mol.Biol.Evol. 19(12): 2176-2190.
Benson, W.W. (1972) Natural selection for Müllerian mimicry in Heliconius erato
in Costa Rica. Science 176: 936-939.
Benson, W.W., Brown, K.S. and Gilbert, L.E. (1975) Coevolution of plants and
herbivores: passion flower butterflies Evolution 29: 659-680.
27
Bond, A.B. and Kamil, A.C. (2002) Visual predators select for crypticity and
polymorphism in virtual prey. Nature 415: 609-613.
Bowers, M.D., Brown, I.L. and Whey, D. (1985) Bird predation as a selective agent
in a butterfly population. Evolution 39: 93-103.
Brower, A.V.Z. (1994) Phylogeny of Heliconius butterflies inferred from
mitochondrial DNA sequences (Lepidoptera: Nymphalidae)
Mol.Phylogenet.Evol. 3:159-174.
Brower, A.V.Z. (1996a) Parallel race formation and the evolution of mimicry in
Heliconius butterflies: A phylogenetic hypothesis from mitochondrial DNA
sequences. Evolution 50(1): 195-221.
Brower, A.V.Z. (1996b) A new mimetic species of Heliconius (Lepidoptera:
Nymphalidae), from southeastern Colombia, as revealed by cladistic analysis
of mitochondrial DNA sequences. Zool.J.Linn.Soc. 116: 317-332.
Brower, A.V.Z. (1997) The evolution of ecologically important characters in
Heliconius butterflies (Lepidoptera: Nymphalidae): a cladistic review.
Zool.J.Linn.Soc. 19: 457-472.
Brower, A.V.Z. and DeSalle, R. (1998) Patterns of mitochondrial versus nuclear
DNA sequence divergence among nymphalid butterflies: the utility of
wingless as a source of characters for phylogenetic inference. Insect
Mol.Biol. 7: 73-82.
Brower, A.V.Z. and Egan, M.G. (1997) Cladistic analysis of Heliconius butterflies
and relatives (Nymphalidae: Heliconiiti): a revised phylogenetic position for
28
Eueides based on sequences from mtDNA and a nuclear gene
Proc.R.Soc.Lond.B 264: 969-977.
Brower, L.P. (1984) Chemical defense in butterflies. In: Vane-Wright.R.I and
Ackery.P.R (eds.). The Biology of Butterflies. Academic Press, New York
pp. 109-134.
Brower, L.P. and Brower, J.V.Z. (1964) Birds, butterflies, and plant poisons: a study
in ecological chemistry. Zoologica 49: 137-159.
Brower, L.P., Brower, J.V.Z. and Collins, C.T. (1963) Experimental studies of
mimicry. 7. Relative palatability and müllerian mimicry among neotropical
butterflies of the subfamily Heliconiinae. Zoologica 48: 65-84.
Brown, K.S. (1979) Ecologia Geográfica e Evolução nas Florestas Neotropicais. 2
vols. (Tese apresentada à Universidade Estadual de Campinas como parte
das exigências de um Concurso de Livre Docência, area de Ecologia).
Universidade Estadual de Campinas, Campinas, Brazil.
Brown, K.S. (1981) The biology of Heliconius and related genera.
Annu.Rev.Entomol. 26: 427-456.
Brown, K.S., Sheppard, P.M. and Turner, J.R.G. (1974) Quaternary refugia in
tropical America: evidence from race formation in Heliconius butterflies
Proc.R.Soc.Lond.B 187: 369-378.
Chai, P. (1986) Field observations and feeding experiments on the response of
rufous-tailed jacamars (Galbula ruficauda) to free-flying butterflies in a
tropical rainforest. Biol. J. Linn. Soc. 29: 161-189.
29
Chai, P. (1988) Wing colouration of free-flying Neotropical butterflies as a signal
learned by a specialized avian predator. Biotropica 20: 20-30.
Chai, P. (1996) Butterfly visual characteristics and ontogeny of responses to
butterflies by a specialized tropical bird. Biol. J. Linn. Soc. 59: 37-67.
Coppinger, R.P. (1969) The effect of experience and novelty on avian feeding
behaviour with reference to the evolution of warning colouration in
butterflies. I. Reactions of wild-caught adult blue-jays to novel insects.
Behaviour 35: 45-60.
Coyne, J.A. and Orr, H.A. (1998) The evolutionary genetics of speciation
Phil.Trans.R.Soc.Lond.B 353: 287-305.
Darwin, C. (1859) On the Origin of Species by Means of Natural Selection, or the
Preservation of Favoured Races in the Struggle for Life. London: John
Murray.
Dawkins, R. (1976) The Selfish Gene, Oxford Univ. Press, Oxford, UK.
Dobzhansky, T. (ed.) (1937) Genetics and the origin of species. Columbia Univ.
Press.
Doi, M., Matsuda, M., Tomaru, M., Matsubayashi, H. and Oguma, Y. (2001) A
locus for discrimination behaviour causing sexual selection in Drosophila.
Proc. Nat. Acad. Sci. USA 98(12): 6714-6719.
Eltringham, H. (1916) On specific and mimetic relationships in the genus
Heliconius. Trans.Entomol.Soc.Lond. pp. 101-148.
Emsley, M.G. (1965) Speciation in Heliconius (Lepidoptera: Nymphalidae):
morphology and geographic distribution. Zoologica (NY) 50: 191-254.
30
Endler, J.A. (1977) Geographic variation, speciation and clines. Princeton Univ.
Press, Princeton, USA.
Engler, H.S., Spencer, K.C. and Gilbert, L.E. (2000) Preventing cyanide release
from leaves Nature 406: 144-145.
Estrada, C. and Jiggins, C.D. (2002) Patterns of pollen feeding and habitat
preference among Heliconius species Ecol.Entomol. 27: 448-456.
Fisher, R.A. (1930) The genetical theory of natural selection. Clarendon, Oxford,
UK.
Gilbert, L.E. (1975) Ecological consequences of a coevolved mutualism between
butterflies and plants. In: Gilbert, L.E., Raven, P.R. eds.. Coevolution of
Animals and Plants. Univ. of Texas Press, Austin, TX, USA. pp. 210-240.
Gilbert, L.E. (2003) Adaptive novelty through introgression in Heliconius wing
patterns: evidence for a shared genetic “tool box” from synthetic hybrid
zones and a theory of diversification, in Ecology and evolution taking flight:
butterflies as model systems, edited by C.L.Boggs, W.B.Watt and
P.R.Ehrlich. Univ. of Chicago Press, Chicago.
Grant, B.R. and Grant, P.R. (1993) Evolution of Darwin’s finches caused by a rare
climatic event. Proc.R.Soc.Lond.B 251: 111-117.
Grant, P.R. (1993) Hybridization of Darwin’s finches on Isla Daphne Major,
Galapagos. Phil.Trans.R.Soc.Lond.B 340: 127-139.
Greenwood, J.J.D., Cotton, P.A. and Wilson, D.M. (1989) Frequency dependent
selection on aposematic prey – some experiments. Biol. J. Linn. Soc. 36(12): 213-226.
31
Guilford, T. (1985) Is kin selection involved in the evolution of warning coloration?
Oikos 45: 31-36.
Guilford, T. (1988) The evolution of conspicuous coloration. Am. Nat. 131: S7-S21.
Guilford, T. (1990) The evolution of aposematism. In: D.L.Evans and J.O.Schmidt
eds. Insect defenses. Adaptive mechanisms and strategies of prey and
predators. State Univ. of New York Press, Albany, NY, USA.
Haldane, J.B.S. (1955) On the biochemistry of heterosis, and the stability of
polymorphism. Proc. R. Soc. Lond. B 144: 217-220.
Harrison, R.G. (1993) Hybrids and hybrid zones: historical perspective. In:
Harrison.R.G. ed. Hybrid zones and the Evolutionary Process. Oxford Univ.
Press, New York, USA pp. 3-12.
Järvi, T., Sillén-Tullberg, B., and Wiklund, C. (1981a) The cost of being
aposometic: an experimental study of predation on larvae of Papilio
machaon by the great tit Parus major. Oikos 36: 267-272.
Järvi, T., Sillén-Tullberg, B., and Wiklund, C. (1981b) Individual versus kin
selection for aposometic coloration: a reply to Harvey and Paxton. Oikos 37:
393-395.
Jiggins, C.D., McMillan, W.O., Neukirchen, N. and Mallet, J. (1996) What can
hybrid zones tell us about speciation? The case of Heliconius erato and
H.himera (Lepidoptera: Nymphalidae). Biol.J.Linn.Soc. 59: 221-242.
Jiggins, C.D. and Mallet, J. (2000) Bimodal hybrid zones and speciation. Trends
Ecol. Evol. 15: 250-255.
32
Jiggins, C.D. and McMillan, W.O. (1997) The genetic basis of an adaptive radiation:
warning colour in two Heliconius species. Proc. R. Soc. Lond. B 264: 11671175.
Jiggins, C.D., Naisbit, R.E., Coe, R.L. and Mallet, J. (2001a) Reproductive isolation
caused by colour pattern mimicry. Nature (Lond.) 411: 302-305.
Jiggins, C.D., Linares, M., Naisbit, R.E., Salazar, C., Yang, Z. and Mallet, J.
(2001b) Sex-linked hybrid sterility in a butterfly. Evolution 55: 1631-1638.
Kapan, D.D. (2001) Three-butterfly system provides a field test of müllerian
mimicry, Nature 409: 338-340.
Lee, C.S., McCool, B.A., Moore, J.L., Hillis, D.M. and Gilbert, L.E. (1992)
Phylogenetic study of heliconiine butterflies based on morphology and
restriction analysis of ribosomal RNA genes. Zool.J.Linn.Soc. 106: 17-31.
Leimar, O., Enquist, M. and Sillén-Tullberg, B. (1986) Evolutionary stability of
aposometic coloration and prey unprofitability: a theoretical analysis. Am.
Nat. 128: 469-490.
Linares, M. (1996) The genetics of the mimetic coloration in the butterfly
Heliconius cydno weymeri. J.Hered. 87: 142-149.
Linares, M. (1997) The ghost of mimicry past: laboratory reconstitution of an
extinct butterfly ‘race’ Heredity 78: 628-635.
Mallet, J., Neukirchen,W. and Linares, M. (2002) Hybrids between species of
Heliconius and Euides butterflies: a database.
http://www.ucl.ac.uk/taxome/hyb/
33
Mallet, J. (1993) Speciation, Raciation, and Color pattern Evolution in Heliconius
Butterflies: Evidence from Hybrid Zones, In R.G.Harrison (ed.): Hybrid
zones and the evolutionary process. Oxford Univ. Press, NY. pp. 226-260.
Mallet, J. (1989) The genetics of warning colour in Peruvian hybrid zones of
Heliconius erato and H. melpomene. Proc.R.Soc.Lond.B 236: 163-185.
Mallet, J. and Barton, N.H. (1989) Strong natural selection in a warning colour
hybrid zone. Evolution 43: 421-431.
Mallet, J. and Gilbert, L.E. (1995) Why are there so many mimicry rings?
Correlations between habitat, behaviour and mimicry in Heliconius
butterflies Biol.J.Linn.Soc 55: 159-180.
Mallet, J., Jiggins, C.D. and McMillan, W.O. (1998a) Mimicry and warning colour
at the boundary between races and species. In Howard, D.J. and Berlocher,
S.H. (eds.) Endless Forms: Species and Speciation. Oxford University Press.
pp.390-403.
Mallet, J., McMillan, W.O., and Jiggins, C.D. (1998b). Estimating the mating
behaviour of a pair of hybridizing Heliconius species in the wild. Evolution
52: 503-510.
Mayr, E. (1963) Animal Species and Evolution. Belknap, Cambridge, MA.
Muller, F. (1879) Ituna and Thyridia; a remarkable case of mimicry in butterflies
Trans. Ent. Soc. Lond. xx-xxix.
Naisbit, R.E., Jiggins, C.D. and Mallet, J. (2001) Disruptive sexual selection against
hybrids contributes to speciation between Heliconius cydno and Heliconius
melpomene. Proc.R.Soc.Lond.B 268: 1-6.
34
Naisbit, R.E. (2001) Ecological divergence and speciation in Heliconius cydno and
H. melpomene. Doctoral dissertation, University College London, London,
UK.
Naisbit, R.E., Jiggins, C.D., Linares, M., Salazar, C. and Mallet, J. (2002) Hybrid
sterility, Haldane’s rule, and speciation in Heliconius cydno and H.
melpomene. Genetics 161: 1517-1526.
Palopoli, M.F. and Wu, C.I. (1994) Genetics of hybrid male sterility between
Drosophila sibling species – A complex web of epistasis is revealed in
interspecific studies, Genetics 138(2): 329-341.
Pinheiro, C.E.G. (1996) Palatability and escaping ability in Neotropical butterflies:
tests with wild kingbirds (Tyrannus melancholicus, Tyrannidae). Biol. J.
Linn. Soc. 59: 351-365.
Pinheiro, C.E.G. (1997) Unpalatability, mimicry and escaping ability in neotropical
butterflies: experiments with wild predators. Doctoral dissertation,
University of Oxford, Oxford, UK.
Poulton, E.B. (1890) The Colours of Animals. London: Kegan Paul, Trench, Trübner
& Co Ltd pp. 46-47.
Ritland, D.B. (1998) Mimicry-related predation on two viceroy butterfly (Limenitis
archippus) phenotypes. Am. Mid. Nat. 140(1): 1-20.
Saetre, G.P., Moum, T., Boures, S., Kral, M., Adamjam, M. and Moreno, J. (1997)
A sexually selected character displacement in flycatchers reinforces
premating isolation. Nature 387: 589-592.
35
Schlenoff, D.H. (1985) The startle responses of blue jays to Catocala (Lepidoptera:
Noctuidae) prey models. Anim. Behav. 33: 1057-1067.
Schluter, D. (2001) Ecology and the origin of species. Trends Ecol. Evol. 16: 372380.
Seehausen, O., van Alphen, J.J. and Witte, F. (1997) Cichlid fish diversity
threatened by eutrophication that curbs sexual selection. Science 277: 18081811.
Servedio, M.R. (2000) The effects of predator learning, forgetting, and recognition
errors on the evolution of warning coloration, Evolution 54(3): 751-763.
Sheppard, P.M., Turner, J.R.G., Brown, K.S., Benson, W.W. and Singer, M.C.
(1985) Genetics and the evolution of mullerian mimicry in Heliconius
butterflies. Phil.Trans.R.Soc.Lond.B 308: 433-613.
Sillén-Tullberg, B. (1985) Higher survival of an aposometic than of a cryptic form
of a distasteful bug. Oecologia 67: 411-415.
Smiley, J.T. (1978a) The host plant ecology of Heliconius butterflies in
Northeastern Costa Rica. Doctoral dissertation, University of Texas at
Austin, Austin TX, USA.
Smiley, J.T. (1978b) Plant chemistry and the evolution of host specificity: new
evidence from Heliconius and Passiflora. Science 201: 745-747.
Sota, T. and Vogler, A.P. (2001) Incongruence of Mitochondrial and Nuclear Gene
Trees in the Carabid Beetles Ohomopterus. Syst. Biol. 50(1): 39-59.
Speed, M.P. (1999) Robot predators in virtual ecologies: the importance of memory
in mimicry studies. Anim. Behav. 57: 203-213.
36
Stratton, G.E. and Uetz, G.W. (1986) The inheritance of courtship behaviour and its
role as a reproductive isolating mechanism in two species of Schizocosa wolf
spiders (Aranae; Lycosidae). Evolution 40: 129-141.
Swanson, H.F. and Monge-Najera, J. (2000) The effects of methodological
limitations in the study of butterfly behaviour and demography: a daily study
of Vanessa atalanta (Lepidoptera: Nymphalidae) for 22 years Revista de
Biologia Tropical 48(2-3): 605-613.
Tullrot, A. (1994) The evolution of unpalatability and warning coloration in softbodied marine invertebrates. Evolution 48: 925-928.
Turner, E.R.A. (1961) Survival values of different methods of camouflage as shown
in a model population. Proc. Zool. Soc. Lond. 136: 273-284.
Turner, J.R.G. (1981) Adaptation and evolution in Heliconius: A defense of
NeoDarwinism. Ann. Rev. Ecol. Syst. 12: 99-121.
Turner, J.R.G. (1984) Mimicry: the palatability spectrum and its consequences. In:
R.I.Vane-Wright and P.R.Ackery, eds. The biology of butterflies. Academic
Press, NY, USA pp. 141-162.
Turner, J.R.G., Kearnet, E.P. and Exton, L.S. (1984) Mimicry and the Monte Carlo
predator: the palatability spectrum and the origins of mimicry. Biol. J. Linn.
Soc. 23: 247-268.
Via, S. (2001) Sympatric speciation in animals: the ugly duckling grows up. Trends
Ecol. Evol. 16: 381-390.
Waldman, B. and Adler, K. (1979) Toad tadpoles associate preferentially with
siblings. Nature 282: 611-613.
37
Weale, M.E., Whitwell, D., Raison, H.E., Raymond, D.L. and Allen, J.A. (2000)
The influence of density on frequency dependent food selection: a
comparison of four experiments with wild birds. Oecologia 124: 391-395.
Wiklund, C. and Järvi, T. (1982) Survival of distasteful insects after being attacked
by naïve birds: a reappraisal of the theory of aposematic coloration evolving
through individual selection. Evolution 36: 998-1002.
38