Introduction
The diversity of color patterns found in the Heliconius butterfly
radiation is a striking example of the power of natural selection to
generate biodiversity. However, while the most popular theory describing
the evolution of these vivid color patterns proposes a framework
dissuading from wing pattern diversity, we in fact find dozens of
established color patterns throughout the neotropics
(Müller, 1879;
Joron and Mallet 1998; Mallet and Joron 1999; Moest et al., 2020).
Franz Müller (1879),
suggested in his theory that mimicking organisms which are unpalatable,
venomous or toxic to predators, benefit from reduced predation by
converging on common warning patterns. As these organisms become all the
more similar over time, Müllerian mimicry theory predicts that the
weight of predation will be optimally shared amongst the mimicking
populations. Furthermore, the evolution of stark warning colorations
(aposematism), increases the effectiveness of this evolutionary strategy
by providing memorable patterns and colors to predators
(Su et al., 2015). Examples
of animals that through natural selection have trodden this evolutionary
journey are familiar to many of us for their striking aspects
(pitvipers, poison-dart frogs, bumblebees and wasps
(Sanders et
al., 2006; Symula et al., 2001; Williams, 2007; Boppré et al., 2017).
The main mechanism driving this mimicry is known as positive
frequency-dependent selection (pFDS), where the most common warning
signal is more likely to spread through a population as it will be the
most avoided by predators
(Müller, 1879). In the past
decades, empirical evidence has largely validated pFDS to be a principal
selective force maintaining such phenotypic convergence throughout the
animal kingdom
(Mallet
and Barton, 1989; Symula et al., 2001; Dumbacher and Fleischer, 2001;
Sanders et al., 2006; Noonan and Comeault, 2009; Borer et al., 2010;
Miller and Pawlik, 2013; Chouteau et al., 2016).
Heliconius butterflies are a renowned example of Müllerian mimicry.
However, as first described by Henry Walter Bates (1862), the genus
clearly demonstrates a diverse array of warning color patterns
established throughout several mimicry rings. This presents a challenge
to Müller’s theory which predicts that the selective pressures enacted
by predators attacking novel color patterns should force the convergence
of many warning signals into few easily recognizable color patterns. In
contrast to this expectation, the co-mimics Heliconius erato andHeliconius melpomene diverged into over 25 geographic color
pattern morphs.
(Bates, 1862;
Turner, 1975; Mallet and Gilbert 1995; Van Belleghem et al., 2020).
These mimicry rings maintain homogenous local warning color patterns
within their borders through localized pFDS mostly driven by a few
insectivorous birds such as rufous-tailed Jacamars and
tyrant-flycatchers
(Benson,
1972; Chai, 1986; Langham, 2004; Mallet and Barton, 1989; Pinheiro,
2011). However, at the boundaries of these mimicry rings hybridization
frequently occurs and results in narrow regions of intermediate color
patterns (Mallet,
1986a; Thurman et al., 2019; Edelman et al., 2019). Such phenomena can
also be observed in vertebrate Müllerian mimics such as the dendrobatid
poison-dart frog radiation (Roland et al., 2017).
In contrast to the homogenous local warning color patterns, some species
have evolved the ability to maintain multiple mimetic warning phenotypes
in a single population, a phenomenon known as “polymorphic mimicry”
(O’Donald and Pilecki,
1970). In these populations, distinct morphs are locally adapted to
their environment by sharing distribution with other Müllerian co-mimics
(Arias et al., 2016). The
selective pressures that allow polymorphic mimicry to evolve and be
maintained remains a largely unresolved question. Historically,
polymorphy was considered to be a random occurrence with no obvious
advantages to the organism bearing it. However, initial evidence in
banded land snails (Cain and
Sheppard, 1954) and later in a variety of other organisms such as
spiders, guppies and wolves
(Hendrickx et al.,
2015; Hedrick et al., 2016; Hughes et al., 2013), has indicated that
polymorphism may serve an adaptive role that can be maintained through
sexual selection and possibly promote speciation
(Jamie and Meier, 2020).
Such a system has been described in Heliconius numata , where
polymorphism is considered the result of competing selective pressures
on the genomic architecture underlying the trait
(Jay et al., 2021).
In this study with test sites throughout Central and South America, we
set out to characterize the ecological pressures that drive polymorphism
in aposematic butterflies. The Müllerian mimic Heliconius dorisis known for being polymorphic across its entire geographic distribution
that spreads across most of South and Central America
(Mallet, 1999;
Constantino et al., 2005), with both red and blue color morphs found
throughout its range. While these two morphs are ubiquitous to allH. doris populations, personal observations point out blue morphs
being more abundantly found than red morphs in coastal areas of French
Guiana. Additionally, red morphs show a divergence in the red rayed
pattern where rays have a broader shape in Central America where red
banded co-mimics are common and thinner rays in South America which
perfectly match those of the thin red ray mimicry ring of the amazon
basin (see Figure 1). Here, we tested if red and blue morphs of H.
doris reflect predictions of a balanced polymorphism, where we expected
both morphs to experience similar predation pressure wherever they are
both local. We also used the regional difference in the red H.
doris morphs between South and Central America to assess the ability of
pFDS to drive adaptive divergence of a balanced polymorphism at varying
geographic scales. Furthermore, we tested if the differences in co-mimic
frequency in French Guiana from rayed phenotypes in the interior to
non-rayed on the coast (Blum,
2008), can drive local differences in predation on H. dorismorphs.
Even though Müllerian Mimicry theory predicts warning signal monomorphy
over time, we have found the selective pressures that allow H.
doris to maintain multiple warning colors across its range. We
have further observed how the same selective forces maintaining this
polymorphism also act to drive divergence in warning coloration at large
geographical scales.