The paradox of polymorphic mimicry in H. doris
The strong selective forces that drive Müllerian mimicry are predicted
to result in monomorphism among mimicking species, yet as in H.
doris , there are many examples of polymorphic mimicry in nature. Our
study sheds some light on how this paradox may be achieved. Our results
suggest that pFDS can vary at regional scales, and is constrained to
knowledgeable predator communities which are savvy to the aposematic
forms found only in their local ecosystem
(Chouteau et al., 2016;
Langham, 2004). For example, over the relatively short distance of
~30km, we found significant differences in the attacks
on native red morphs of H. doris , with significantly less attacks
occurring at the sites where other red co-mimics are present. This
suggests the predator community knowledge was quite distinct at the
different sites and corresponds to reports of Jacamars having rather
narrow home ranges (Chai,
1986). However, this begs the question of “how do the red H.
doris persist in areas lacking red co-mimics?”, as we would expect the
lack of co-mimics to result in higher predation and eventual removal of
the red morph from the population.
A possible explanation lies in the dispersal behaviour from nearby
populations where red co-mimics are present and the red H. dorismorphs have greater protection. Other Heliconius species such asH. erato and H. melpomene have an estimated dispersal
range of only ~2.5-5km
(Mallet, 1986a; Mallet
et al., 1990), as a result of their “trap-line” behaviors as adults
(Young & Montgomery, 2020).
However, it has been suggested that Heliconius doris may
disperse much larger distances immediately post pupal eclosion, which
could reduce chances of sib-competition and sib-matings
(Mallet, 1999).Heliconius doris females are known to gather in groups and lay
eggs on single plants, often even the same leaf, which we observed
first-hand in French Guiana. This results in a mass of gregarious larvae
that will often fully consume all leaves and tendrils on thePassiflora host. After consumption, an individual host plant can
require several years to reach a size sufficient to host another
population of H. doris eggs. It would then likely benefit newly
eclosed females to disperse larger distances than otherHeliconius species that tend to oviposit much fewer eggs in close
proximity. Therefore, it is possible that group egg laying, and
relatively greater dispersal in H. doris could drive a
“mismatch” of warning colors in the distribution of Heliconiusco-mimetic species, as seen in French Guiana. This dispersal-based
hypothesis would result in sink populations for H. doris morphs,
where the red co-mimics are lacking, that are continuously replenished
from source populations where red morphs have greater protection. It is
difficult to understand how this could be an evolutionarily stable
strategy and dispersal data for H. doris are lacking to support
such a source-sink model for the presence of red H. doris morphs
where the co-mimics are absent.
Another important aspect that could explain the distribution of red
morphs and polymorphic mimicry in H. doris is the genetic basis
for the color variation. In H. numata, polymorphic color patterns
result from allelic changes at a single locus, P(Joron et al., 2006). More
specifically, the different color patterns result from varying
combinations of chromosomal inversions across the P locus
(Joron et al., 2011). The
color pattern variation is maintained in local populations through
disassortative mating
(Maisonneuve et al., 2021),
a form of negative frequency-dependent selection where rare morphs are
preferred mates resulting in offspring of variable colorations. Since
the color pattern differences are controlled by a single locus, and the
different alleles cannot recombine due to the inverted orientations
(Jay et al., 2021),
disassortative mating will keep producing color pattern variation in
perpetuity. In H. numata , each of the different color patterns
also correspond to local co-mimics, and different morphs appear to share
similar predation pressures
(Chouteau et al., 2016). We
propose that a similar system may have evolved in H. doris , with
non-recombining alleles at a single locus controlling color pattern
variation coupled with disassortative mating as such a system would
result in distinct red and blue morphs in each generation across theH. doris range. Currently, there is no data for the inheritance
of color patterns or mate preference in H. doris , which would be
vital for determining how polymorphic mimicry is maintained in the
species.