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Edited by: It is generally accepted that butterfly wing color-patterns have ecological and behavioral
Igor Kovalchuk, University of
functions that evolved through natural selection. However, particular wing color-patterns
Lethbridge, Canada
may be produced physiologically in response to environmental stress, and they may lack
Reviewed by:
Olga Kovalchuk, University of significant function. These patterns would represent an extreme expression of phenotypic
Lethbridge, Canada plasticity and can eventually be fixed genetically in a population. Here, three such cases in
Carmel Mothersill, McMaster butterflies are concisely reviewed, and their possible mechanisms of genetic assimilation
University, Canada
are discussed. First, a certain modified color-pattern of Vanessa indica induced by tem-
*Correspondence:
perature treatments resembles the natural color-patterns of its closely related species of
Joji M. Otaki , Department of
Chemistry, Biology and Marine the genus Vanessa (sensu stricto). Second, a different type of color-pattern modification
Science, Faculty of Science, can be induced in Vanessa cardui as a result of a general stress response. This modified
University of the Ryukyus, 1 Senbaru, pattern is very similar to the natural color-pattern of its sister species Vanessa kershawi.
Nishihara, Okinawa 903-0213, Japan.
Third, a field observation was reported, together with experimental support, to show that
e-mail: otaki@sci.u-ryukyu.ac.jp
the color-pattern diversity of a regional population of Zizeeria maha increased at the north-
ern range margin of this species in response to temperature stress. In these three cases,
modified color-patterns are unlikely to have significant functions, and these cases suggest
that phenotypic plasticity plays an important role in butterfly wing color-pattern evolution.
A neutral or non-functional trait can be assimilated genetically if it is linked, like a parasitic
trait, with another functional trait. In addition, it is possible that environmental stress causes
epigenetic modifications of genes related to color-patterns and that their transgenerational
inheritance facilitates the process of genetic assimilation of a neutral or non-functional trait.
Keywords: butterfly wing, color-pattern, epigenetic modification, genetic assimilation, neutral or non-functional
trait, phenotypic plasticity, speciation, stress response
the color-pattern evolution of butterflies. In addition to syn- high. In contrast, V. indica is widely distributed in Asia. It has been
thetic compilations of possible cases of plasticity-related evolu- speculated that the ancestral species of the Indonesian Vanessa
tion (Schlichting and Smith, 2002; West-Eberhard, 2003; Badyaev, were exposed to a natural “temperature treatment,” showing color-
2005), results that demonstrate a role of phenotypic plasticity and pattern modifications as a side-effect, and subsequently adapted
genetic assimilation in evolution have also been reported recently to those environments (Otaki, 2008c). A similar hypothesis can be
from field studies of different organisms (Aubret and Shine, 2009; proposed in the atalanta group, in which V. tameamea is endemic
Buckley et al., 2010; Scoville and Pfrender, 2010; Muschick et al., to mountainous areas of the Hawaiian islands, whereas its sister V.
2011). atalanta is widely distributed in Europe and North America (Otaki
In many cases, it appears that color-patterns have evolved as a et al., 2006; Otaki, 2008c).
result of an environmental stress response. We have focused partic- The Vanessa case is highly informative in that there may be an
ularly on the genus Vanessa (Otaki and Yamamoto, 2004a,b; Otaki environmental role in the color-pattern evolution of nymphalid
et al., 2006; Otaki, 2007a, 2008a,b,c) and, to a lesser extent, on the butterflies beyond Vanessa. A distinct feature of the TS-type mod-
genus Junonia (Otaki et al., 2005; Otaki, 2007b, 2008a; Mahdi et al., ifications is a simplified overall color-pattern, especially a compro-
2011). In addition, we recently discovered an intriguing field case mised eyespot and parafocal element (Nijhout, 1984; Otaki, 1998,
in which phenotypic plasticity in response to environmental stress 2009; Otaki and Yamamoto, 2004a). Similar phenotypes can be
contributes to the color-pattern evolution of the pale grass blue, observed to occur relatively widely in the natural color-patterns of
Zizeeria maha (Otaki et al., 2010). nymphalid butterflies (Figure 1).
In this paper, we briefly review important information obtained
from these studies and specify the topics that must be fur- EVOLUTION OF VANESSA CARDUI AND VANESSA KERSHAWI
ther examined to accurately understand this interesting and far- The TS-type modifications can be induced not only by temper-
reaching phenomenon in biology. The possible contribution of ature conditions but also by certain chemicals, such as sodium
epigenetic changes and their transgenerational inheritance to the tungstate (Otaki, 1998) and dextran sulfate (Serfas and Carroll,
evolution of color-patterns is also discussed. 2005). However, it is important to stress that the TS-type does not
the outward type. The TS-type outbreak lasted a few years and
spanned at least 10 generations. It is probable that the TS-type
modifications were genetically assimilated in the population at SIDE-EFFECT MODEL AND EPIGENETIC INHERITANCE
that time. SIDE-EFFECTS ALLOW NON-FUNCTIONAL OR NEUTRAL TRAITS TO BE
After a rearing system was established for this species (Hiyama ASSIMILATED GENETICALLY
et al., 2010), this genetic assimilation process was reproduced in a There are several possible mechanistic explanations for these
laboratory experiment (Otaki et al., 2010). Although the natural plasticity-oriented evolutionary cases. The so-called “side-effect
population later became nearly extinct, it is remarkable that the model” was proposed to explain the evolution of Vanessa (Otaki,
modified individuals strongly resemble other lycaenid species that 2008c). This model first makes the reasonable assumption that
inhabit relatively cold areas (Otaki and Yamamoto, 2003; Otaki Vanessa is a group of species that favor a temperate environment
et al., 2010; Figure 3). The modified color-patterns observed in this and are not highly resistant to temperature shock. In addition,
population were very similar to those seen in Maculinea species it is assumed that the ancestral species of the group had rela-
that live in high mountainous areas (Otaki and Yamamoto, 2003), tively high vagility, similar to that of V. indica and V. atalanta.
and the sexually dimorphic response to cold-shock parallels the Due to its vagility, the ancestral species can expand its range
sexually dimorphic color-patterns of Lycaena dispar. margin to tropical areas, but the temperature of these areas is
too high to allow the next generation of the species to be pro- the transgenerational effect of epigenetic traits could involve the
duced. However, even in tropical regions, the species can live three cases discussed above. In Drosophila, epigenetic changes
in mountainous areas where relatively low temperatures occur. are mediated by the formation of a heritable heterochromatin
There, large daily temperature fluctuations serve as natural cold- in response to temperature stress (Seong et al., 2011). Given the
shocks. Natural selection operates to favor cold resistance in prevalence of epigenetic modifications (Jablonka and Raz, 2009),
the isolated Vanessa populations. Color-pattern changes accom- similar molecular mechanisms can be envisioned in butterflies.
pany this increase in cold resistance. However, the changed color Other mechanisms of epigenetic changes, such as DNA methyla-
traits have no functional relationship to cold resistance. Thus, tion, histone modifications, and regulation by non-coding RNAs,
color-pattern modifications are an opportunistic side-effect of could also occur.
cold resistance, i.e., color-pattern changes or new color-pattern However, epigenetic changes induced by temperature shock do
traits are “parasitic” to cold resistance (Otaki, 2008c). Specifi- not persist for many generations in Drosophila (Seong et al., 2011).
cally, because the color-pattern changes are induced by a humoral To establish a new trait in a population, a mechanism should exist
factor in the hemolymph known as cold-shock hormone (CSH; to genetically fix such a new trait into the DNA sequences. If the
Mahdi et al., 2010, 2011), the ability to efficiently secrete CSH cold-shock resistance itself is epigenetically inherited, this form
into the hemolymph may be directly related to cold resistance of inheritance allows the population to develop resistance rela-
and may be opportunistically linked to color-pattern modifi- tively rapidly and results in a higher probability of survival and
cations. As a result, neutral or non-functional color-patterns of avoidance of extinction for the population. This process fur-
may be fixed in a population through a process of genetic nishes an opportunity for the natural selection of stress-induced
assimilation. phenotypes, because the operation of natural selection requires a
To support this model, studies of the relationship of temper- relatively high number of generations. This process could even-
ature to Vanessa’s life history, behavior, and physiology must be tually cause the assimilation of a new trait in the population and
conducted. Further clear identification of the CSH is required. could ultimately promote speciation.
Hopefully, the genetic assimilation of the plastic phenotype will It is important to emphasize that the new trait discussed
be reproduced in the laboratory, although rearing Vanessa for gen- above need not be a functional trait. It can be neutral or non-
erations in an artificial environment would be relatively difficult functional (Otaki, 2008c). Neutral or non-functional traits will
from a technical perspective. create opportunities for subsequent functional evolution. If all
A fundamentally similar history may be hypothesized in the traits were fully functional, subsequent evolution would only dam-
case of V. cardui and V. kershawi, although different molecular age functional traits, leading to the deterioration of the species.
pathways may be involved in the color-pattern modifications of In this sense, neutral or non-functional traits have an evolu-
these species. It is probable that the common ancestor had color- tionary “function” as a source of opportunities for subsequent
patterns and phenotypic plasticity similar to those of V. cardui, a evolution and speciation. This concept is similar to the idea that
cosmopolitan species. As this ancestral species invaded a relatively neutral mutations “function” by furnishing a foundation for sub-
arid environment, stress resistance developed over the generations sequent evolutionary adaptation at the molecular level (Wagner,
through natural selection. As a side-effect, color-pattern modifi- 2008).
cations occurred and were eventually genetically assimilated in the
population. CONCLUDING REMARKS
Similarly, in the case of Z. maha, the northward migration The three cases of evolution presented in this paper involve coping
selected for cold resistance. As a side-effect, the color-patterns were with environmental stress and the emergence of extreme pheno-
modified at the previous northern margin of the range even before types. The coincidence between physiologically induced pheno-
the population reached the Fukaura area. Although the modified types in a species and the normal phenotypes of related species
traits were not well assimilated in the population at the previ- that live in“stressful”environments is striking. These cases demon-
ous northern margin of the range, a small number of individuals strate the involvement of phenotypic plasticity in evolution. Exper-
migrated farther to the north and established a regional popula- imental demonstration and field observation are further required
tion in the Fukaura area. It is probable that this population was to convincingly demonstrate the roles of phenotypic plasticity and
genetically unstable and that this instability produced an outbreak environmental stress in the color-pattern evolution and specia-
of unstable TS-type modifications. tion of butterflies. Theoretical frameworks are also expected to
emerge from these considerations (Behera and Nanjundiah, 2004;
EPIGENETIC TRAITS COULD FACILITATE STRESS ADAPTATION Lande, 2009; Danchin et al., 2011; Espinosa-Soto et al., 2011; Fierst,
The proposed opportunistic link between stress resistance and 2011).
color-patterns has not yet been demonstrated. If there is no We do not yet accurately know how plastic phenotypes are
such link, it would be difficult for the modified color-patterns genetically assimilated in a given butterfly population to produce
to evolve by natural selection because it is probable that they an independent species, nor do we know the possible roles of epige-
are functionally neutral at best. It is even more probable that netic inheritance in the evolution of butterfly color-patterns. The
these color-patterns are selectively inferior to the normal pat- active role of phenotypic plasticity in evolution is a concept that
terns. An alternative explanation is that stress-induced traits in has gained popularity relatively recently in biology (Pigliucci and
a given generation are heritable in the next generation. These Murren, 2003; Pigliucci et al., 2006; Pfennig et al., 2010) despite its
two explanations are not mutually exclusive. It is possible that original formulation in the 1940s (Waddington, 1942). Epigenetic
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isolated sister taxa. Syst. Entomol. 36, conducted in the absence of any com- Citation: Hiyama A, Taira W and Copyright © 2012 Hiyama, Taira and
362–370. mercial or financial relationships that Otaki JM (2012) Color-pattern evolu- Otaki. This is an open-access article dis-
West-Eberhard, M. J. (2003). Develop- could be construed as a potential con- tion in response to environmental stress tributed under the terms of the Cre-
mental Plasticity and Evolution. New flict of interest. in butterflies. Front. Gene. 3:15. doi: ative Commons Attribution Non Com-
York, NY: Oxford University Press. 10.3389/fgene.2012.00015 mercial License, which permits non-
Received: 01 December 2011; accepted: This article was submitted to Frontiers in commercial use, distribution, and repro-
Conflict of Interest Statement: The 23 January 2012; published online: 06 Epigenomics, a specialty of Frontiers in duction in other forums, provided the
authors declare that the research was February 2012. Genetics. original authors and source are credited.