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Milkweed butterflies (Lepidoptera: Nymphalidae: Danainae) are chemically defended and aposematic (Ackery and Vane Wright 1984). The chemical ecology of several species have been studied extensively, including the iconic and highly migratory Monarch Butterfly, Danaus plexippus (Brower and Glazier 1975; Boppré 1993). Danaine larvae feed on chemically defended plants from which they also extract phytochemical protection.
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Kleptopharmacophagy: Milkweed
butterflies scratch and imbibe from
Apocynaceae-feeding caterpillars
Manuscript received 16 February 2021; revised 15 June 2021;
accepted 8 July 2021; final version received 5 September 2021.
Corresponding Editor: John Pastor.
School of Life and Environmental Sciences, University of
Sydney, Sydney, New South Wales 2006 Australia.
Department of Ichthyology, Australian Museum Research
Institute, Australian Museum, 1 William Street, Sydney, New
South Wales 2010 Australia.
829 Upper Bukit Timah Road, Singapore, 678187
Biological and Earth Sciences, South Australian Museum,
Adelaide, South Australia 5000 Australia.
Biology Department, City College of New York, City
University of New York, New York, New York 10031 USA.
Ph.D. Program in Biology, Graduate Center, City University
of New York, New York, New York 10016 USA.
Entomology Section, National Museum of Natural History,
1000 Manila, Philippines.
Citation: Tea, Y.-K., J. W. Soong, E. P. Beaver, and D. J.
Lohman. 2021. Kleptopharmacophagy: Milkweed butterflies
scratch and imbibe from Apocynaceae-feeding caterpillars.
Ecology 00(00):e03532. 10.1002/ecy.3532
Key words: behavior; leaf-scratching; pharmacophagy; pyrroli-
zidine alkaloids.
Milkweed butterflies (Lepidoptera: Nymphalidae:
Danainae) are chemically defended and aposematic
(Ackery and Vane-Wright 1984). The chemical ecology
of several species have been studied extensively, includ-
ing the iconic and migratory Monarch Butterfly, Danaus
plexippus (Brower and Glazier 1975, Boppr
e 1993).
Danaine larvae feed on chemically defended plants from
which they also extract phytochemical protection. Adult
males of many species supplement their existing bio-
chemical deterrents with pyrrolizidine alkaloids (here-
after, alkaloids) obtained by scratching alkaloid-
containing substrates and imbibing the resulting exu-
dates. These alkaloids impart additional protection to
males, serve as a biochemical precursor for mating pher-
omones, and function as a nuptial gift to females
delivered in the spermatophore (Boppr
e 1990). Here, we
report novel observations from Sulawesi of adult male
danaine butterflies scratching other danaine butterfly
larvae and imbibing the exudates with their proboscis,
presumably to steal their host-plant-derived alkaloids.
While the use of alkaloids as chemical defenses in
insects is not uncommon, it is most conspicuous in the
Lepidoptera, especially in the Danainae, which com-
prises three tribes: Danaini, Ithomiini, and Tellervini
(considered by some to be subfamilies; Lamas 2004).
Danaine species use alkaloids for defense and phero-
mone production (Edgar and Caulvenor 1974, Boppr
1986, Orr et al. 1996). Host-plant-derived chemical
defense is ubiquitous among the Danainae, and mem-
bers of this group participate in diverse mimicry rings
involving poisonous models and palatable non-danaine
mimics wherever they occur (Parsons 1998, Joshi et al.
2017, Nishida 2017).
Pyrrolizidine alkaloids are naturally occurring hepato-
toxic plant secondary metabolites commonly found in
the families Boranginaceae, Apocynaceae, Asteraceae,
Fabaceae, Orchidaceae, and Solanaceae (Wink 1988,
2003, El-Shazly and Wink 2014). Danaine butterflies
either feed on these plants as larvae or seek and imbibe
alkaloids as adults for purposes other than primary
metabolism (pharmacophagy; Boppr
e 1984). In the
Ithomiini, larval host plants are frequently species of
Solanaceae and Apocynaceae (Trigo et al. 1996, Will-
mott and Freitas 2006), whereas in the Tellervini and
Danaini, these are mostly plants from the families
Apocynaceae and Moraceae (Ackery and Vane-Wright
1984). Adult pharmacophagy is less taxon-specific, and
alkaloids are sequestered from a wide variety of sources,
including flowers, damaged or withered leaves, and dried
seed pods of alkaloid-producing plants (all authors per-
sonal observations; Edgar and Caulvenor 1974, Trigo
et al. 1996). Plants in the genera Senecio (Asteraceae),
Heliotropium (Boraginaceae), and Crotalaria (Fabaceae)
are among the most popular targets, consisting mostly
of the alkaloids retronecine and heliotridine (Smith and
Culvenor 1980, Boppr
e 1990). Individual plants in the
Asteraceae genus Senecio, for example, may comprise as
much as 18% in alkaloids by dry mass (Molyneux and
Johnson 1984).
For adult butterflies, alkaloids are used for more than
just chemical defense. They are important precursors for
pheromone production, particularly for the biosynthesis
of danaidone and hydroxydanaidal (Schulz 1998). In
danaine butterflies, males may possess two types of
androconial organs: a pair of eversible abdominal hair-
pencils and a pair of alar glands (sex brands; Ackery and
Vane-Wright 1984, Boppr
e and Vane-Wright 1989).
During pre-copulation, males hover over receptive
Article e03532; page 1
The Scientific Naturalist
Ecology, 0(0), 2021, e03532
©2021 by the Ecological Society of America
females with hairpencils extruded and splayed, dissemi-
nating pheromones that are detected by females (Brower
et al. 1965, Honda et al. 2016). Courtship success corre-
lates with mating success and fecundity (Edgar and
Caulvenor 1974, Honda et al. 2018), and males often
transfer alkaloids to females through spermatophores as
nuptial gifts (Boppr
e 1990). While alkaloids are often
ingested in leaves consumed by caterpillars during the
larval stages, they may be stored as intermediary com-
pounds (Orr et al. 1996) and are not always transferred
to the adult stage (Boppr
e 1990). Withered and dried
parts of alkaloid-producing plants are a favorite of
danaine butterflies, possibly due to higher concentra-
tions and retention of alkaloids. Fresh leaves and other
vegetative parts are also a target in the absence of dried
or withered leaves. Unique to the danaine butterflies
is the unusual behavior known as leaf-scratching
e 1983), in which adult butterflies damage plant
parts with their sharp tarsal claws, liberating plant juices
and sap to imbibe.
Rarely, danaines have been reported imbibing fluids
directly from carcasses of alkaloid-storing insects, though
this phenomenon has been reported infrequently. For
example, in Africa, Danaus chrysippus has been observed
to feed on juices of moribund pyrgormorphid grasshop-
pers that have previously fed on alkaloid-producing
plants, apparently taking advantage of their carcasses as
an alternative source of alkaloids (Owen 1971, Bernays
et al. 1977). This behavior has been observed indepen-
dently by the authors Y. K. Tea and J. W. Soong in Singa-
pore. Both observations involved adults of Parantica
agleoides agleoides (Nymphalidae: Danainae) feeding
from dead lepidopteran carcasses, the pupa of another
danaine species in one case, and a dead arctiine moth in
the other (Fig. 1A). Whether the butterflies were actively
imbibing alkaloids from these sources is unclear, but
danaine pupae and arctiine moths are both chemically
defended by alkaloids (Rothschild et al. 2008).
On 9 December 2019, however, Y. K. Tea and J. W.
Soong observed adult male danaine butterflies scratch-
ing at living butterfly caterpillars in coastal forests of
Tangkoko Batuangus Nature Reserve, North Sulawesi,
Indonesia (1°34033.2N, 125°09036.1E) and apparently
imbibing fluid from them. The behavior was similar to
danaine leaf-scratching, but the butterflies instead
scratched live Idea blanchardii blanchardii larvae that
were feeding on Parsonsia spp. (Apocynaceae; Fig. 1B
E). Adult butterflies of multiple danaine species were
observed scratching many caterpillars along a stretch of
coastal vegetation (˜500 m long), with mid-to-late-instar
caterpillars appearing to be the preferred targets. The
larvae would contort their bodies rapidly in what
appeared to be futile attempts to deter the persistent
scratching of adults. Adult danaine butterflies were
observed actively imbibing from the wounded and ooz-
ing caterpillars, sometimes in mixed species groups that
would congregate for several hours (Fig. 1D). Feeding
butterflies were often so engrossed that they were oblivi-
ous to being touched by human observers. Subsequent
observations over three days revealed repeated visits by
danaine butterflies to the same wounded larvae. Adults
were also observed scratching and imbibing from dead
FIG. 1. Danaine butterflies imbibing from dead and living Lepidoptera. (A) Parantica agleoides agleoides feeding on an arctiine
moth carcass in Singapore. (BF) Various species of danaine observed in Tangkoko Batuangus Nature Reserve, North Sulawesi
scratching and imbibing from living and dead caterpillars of Idea blanchardii blanchardii. Note everted proboscis in all individuals.
(B) Parantica cleona luciplena; (C) Danaus ismare alba; (D) Danaus ismare alba,Euploea algea kirbyi, and Ideopsis juventa tontolien-
sis; (E) Ideopsis vitrea vitrea; (F) Idea blanchardii blanchardii. Caterpillars are dead in panels C, D, and F, but alive in panels B and
E. Photographs by Akio Takatsuki, G
oran Pettersson, Yi-Kai Tea, Jonathan Wei Soong, and Cheong-Weei Gan.
Article e03532; page 2 THE SCIENTIFIC NATURALIST Ecology, Vol. xx, No. xx
caterpillars, although whether these mortalities were a
direct consequence of harassment and scratching is
unclear. Although multiple danaine species were abun-
dant at this locale, adult butterflies were only observed
scratching larvae of I. blanchardii blanchardii. No larvae
of other danaine species were found. Pupae of I. blan-
chardii blanchardii were also observed in situ, but these
remained unmolested and appeared to be of no interest
to adult butterflies. We also include a photograph of
Idea blanchardii blanchardii feeding on a larval carcass of
its own species taken in 2017 at the same location by an
amateur naturalist (Fig. 1F).
In total, we observed seven danaine butterfly species
scratching larvae, both dead and alive. These were
Danaus ismare alba,Euploea algea kirbyi,Idea blan-
chardii blanchardii,Ideopsis juventa tontoliensis,Ideopsis
vitrea vitrea,Parantica cleona luciplena, and Tirumala
ischmoides ischmoides. All of these species, along with
adults of four other danaines (Danaus genutia leucoglene,
Euploea eupator eupator,Euploea hewitsonii hewitsonii,
and Euploea westwoodii meyeri), were also observed
scratching leaves (Fig. 2AL). All 11 danaine species
scratched leaves intermittently during our hours of
observation, between 09:00 and 14:00, mostly on lactif-
erous vines in the genus Parsonsia and other unidentified
apocynaceous plants. Leaf-scratching was also observed
on trees in the genus Premna (Lamiaceae). While species
of Premna (and most other Lamiaceae) are not known
to produce pyrrolizidine alkaloids, they contain isoxa-
zole alkaloids (Barik et al. 1992) and icetexane diterpe-
nes (Dianita and Jantan 2017). We do not know whether
these compounds are attractive to danaine butterflies or
play roles similar to pyrrolizidine alkaloids. Of the doz-
ens of adult butterflies observed scratching plants or
caterpillars, only one was female (Fig. 2B). Observations
of females engaging in leaf-scratching are unusual, since
it is almost exclusively males that engage in this behav-
ior, often gathered in large aggregations (sometimes
numbering in the hundreds) where they imbibe alkaloids
from suitable plants with fervor (Fig. 2M, N).
Why danaine butterflies harass and scratch caterpillars
at this locale remains unclear. Similarly, it is not known
whether the scratching butterflies are attracted by the lar-
vae, their host plants, or both. One possibility is that
caterpillars feeding on apocynaceous plants at this site
are a more concentrated source of alkaloids compared to
their host plants (see Orr et al. 1996). In addition, the
thin larval integument of Idea blanchardii blanchardii may
permit easier access to alkaloid-containing exudate than
through leaf or pupal scratching. The congeneric Idea
FIG. 2. Danaine butterflies exhibiting leaf-scratching on living or dead plants. Observations from Tangkoko Batuangus Nature
Reserve, North Sulawesi. Observations (MN) from Singapore. (A) Danaus genutia leucoglene; (B) Danaus ismare alba; (C) Euploea
hewitsonii hewitsonii; (D) Euploea eupator eupator; (E) Euploea algea kirbyi; (F) Euploea westwoodii meyeri; (G) Idea blanchardii
blanchardii; (H) Idea blanchardii blanchardii (aberrant coloration); (I) Ideopsis juventa tontoliensis; (J) Ideopsis vitrea vitrea; (K)
Parantica cleona luciplena; (L) Tirumala ishmoides ishmoides; (M) Parantica agleoides agleoides; (N) Danaus genutia genutia. The
Danaus ismare alba individual pictured here (B) is the only female that we observed leaf-scratching in North Sulawesi. Photographs
by Yi-Kai Tea, Jonathan Wei Soong, Cheong-Weei Gan, and Lena Chow.
Xxxxx 0000 THE SCIENTIFIC NATURALIST Article e03532; page 3
leuconoe from Japan is similar in having larvae that feed
exclusively on Parsonsia. Under laboratory conditions,
the pyrrolizidine alkaloids ideamine A and B N-oxides
have been isolated from adults, eggs, and host plants,
demonstrating the acquisition and transfer of alkaloids
directly from the host to the larva in this species (Nishida
et al. 1991, ideamine B is a nor-derivative of parsonsine).
Whether a parallel situation occurs in the Sulawesi ende-
mic I. blanchardii blanchardii is unknown, though this
could explain the preference for live and dead caterpillars
of I. blanchardii blanchardii by adults of the same species,
as well as those of other danaine butterflies at this locale.
We note that while our observations of scratching by
adult butterflies at this locale have been limited to leaves
and caterpillars, we are aware of at least one incident
where this behavior has been performed directly on an
adult butterfly (video available online).
The video, taken
at the same locale in 2017 by Samaisukh Sophasan,
clearly shows a male Ideopsis vitrea vitrea harassing,
scratching, and probing the wings of an adult I. blan-
chardii blanchardii with its proboscis.
The population density of danaine butterflies in the
vicinity may also contribute to more frequent observa-
tions of this previously unknown phenomenon. The
coastal habitat of Tangkoko Batuangus Nature Reserve
in Sulawesi is bordered by dense coastal vegetation that
is replete with Apocynaceae. Species of Danaini were the
dominant group of diurnal Lepidoptera, particularly
those of the genera Danaus,Euploea,Idea,Ideopsis,
Parantica, and Tirumala. One alternative hypothesis is
that the butterflies are attracted to the damaged leaves
left by feeding caterpillars, and as a result are in close
proximity to caterpillars that they inadvertently wound
through leaf-scratching. The wounded caterpillars and
their alkaloid-rich exudates then act as a beacon, draw-
ing the attention of butterflies already in the vicinity.
Continuously overlapping generations in this tropical
habitat may also allow newly eclosed adult butterflies to
observe and learn the larval scratching behavior from
older individuals, resulting in cultural transmission of
this unusual behavior (Whiten 2019). Although we
report the occurrence of 11 species, seven of which were
observed feeding on caterpillars, it is likely that this list
will increase with additional observation.
As far as we are aware, these are perhaps the first
observations of milkweed butterflies apparently obtain-
ing alkaloids from the caterpillars of living, closely
related species rather than plants or the dead carcasses
of insects from different orders. We presume that alka-
loids are transferred from the larvae to the adults, but
this hypothesis requires chemical verification, and we
therefore exercise caution interpreting our observations.
Since the larvae appear to be unwilling participants in
this presumed exchange, we suggest this behavior be
termed kleptopharmacophagy,which highlights that
the chemicals consumed by the adults are stolen from
others. However, since it is not clear whether the cater-
pillar wounds and fatalities were caused by scratching,
the alternative neologisms kairopharmacophagy(feed-
ing on defensive chemicals from wounded caterpillars
detected via eavesdropping)ornecropharma-
cophagy(feeding on defensive chemicals from dead
caterpillars) might also be appropriate. It is not known
whether this behavior occurs elsewhere in the tropics or
is truly restricted to this region. Danaus species of the
Americas, for example, are apparently not known to per-
form leaf-scratching (Ramos et al. 2020, Lawson et al.
2021). It is possible that the dearth of natural history
observations on Sulawesi may have precluded observa-
tions elsewhere on the island (but see Tea et al. 2020).
No specimens were collected during the course of observa-
tions on Sulawesi. Field observations were made with accompa-
niment of our guides, Saka and Yulen, whom we thank.
Cheong-Weei Gan accompanied Y. K. Tea and J. W. Soong dur-
ing field work and provided additional photographs. We thank
Michael F. Braby (ANU, Canberra) for discourse regarding the
observed behavior, and two anonymous reviewers for the con-
structive comments. We thank Akio Takatsuki, G
oran Pet-
tersson, Cheong-Weei Gan, and Lena Chow for providing
additional photographs used in this manuscript. The research
of D. J. Lohman is supported by National Geographic Society
grant WW-227R-17 and NSF grant DEB-1541557.
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Xxxxx 0000 THE SCIENTIFIC NATURALIST Article e03532; page 5
... Alternatively, organisms can specifically take up defensive chemicals from plants via pharmacophagy [7][8][9]. For example, adults of some danaine butterfly species actively incorporate defensive chemicals like pyrrolizidine alkaloids from sources such as dried plant parts [10,11]. While these acquired chemicals confer protection on the individual taking them up, it is less well elucidated whether and how this protection can extend to conspecifics that may not have access to these chemicals directly from the source. ...
... The possibility that chemically defended individuals confer protection from predation on initially undefended conspecifics can be realized via different means. Individuals may acquire such defensive chemicals directly from the ( plant) source or indirectly via intraspecific [10,12] or interspecific [11,13] interactions. Alternatively, after attacking a chemically defended individual, a predator may not attack even chemically undefended conspecifics of the prey if it associates the phenotype with distastefulness by learned aversion or avoidance [14][15][16]. ...
Full-text available
Chemical defense is a widespread anti-predator strategy exhibited by organisms, with individuals either synthesizing or extrinsically acquiring defensive chemicals. In some species, such defences can also be transferred among conspecifics. Here, we tested the effects of pharmacophagy on the defense capability of the turnip sawfly, Athalia rosae , which can acquire neo -clerodane diterpenoids (clerodanoids) via pharmacophagy when having access to the plant Ajuga reptans. We show that clerodanoid access mediates protection against predation by mantids for the sawflies, both in a no-choice feeding assay and a microcosm setup. Even indirect access to clerodanoids, via nibbling on conspecifics that had access to the plant, resulted in protection against predation albeit to a lower degree than direct access. Furthermore, sawflies that had no direct access to clerodanoids were consumed less frequently by mantids when they were grouped with conspecifics that had direct access. Most, but not all, of such initially undefended sawflies could acquire clerodanoids from conspecifics that had direct access to the plant, although in low quantities. Together our results demonstrate that clerodanoids serve as a chemical defense that can also be transferred by interactions among conspecifics. Moreover, the presence of chemically defended individuals in a group can confer protection onto conspecifics that had no direct access to clerodanoids.
Full-text available
Predation is an important selection pressure acting on organisms, with organisms evolving diverse anti-predator strategies to combat it. One such widespread strategy is chemical defense in which organisms either synthesize or extrinsically acquire defensive chemicals. Little is known about the intraspecific transfer of such chemicals and if such chemicals acquired from conspecifics can also serve as defense against predation. Here, we used adults of the turnip sawfly, Athalia rosae , which can acquire neo-clerodane diterpenoids ('clerodanoids') via pharmacophagy after exposure to the plant, Ajuga reptans . We show that clerodanoid access mediates protection against predation by mantids for the sawflies, both in a no-choice feeding assay and a microcosm setup. Moreover, even indirect access to clerodanoids, via nibbling on conspecifics that had access to the plant, resulted in protection against predation albeit to a much lower degree than direct access. Furthermore, sawflies that had no direct access to clerodanoids were less consumed by mantids when they were grouped with conspecifics that had direct access. Most, but not all, of such initially undefended sawflies could acquire clerodanoids from conspecifics that had direct access to the plant, although in low quantities. Together our results demonstrate that clerodanoids serve as chemical defense that can be intraspecifically transferred. Moreover, the presence of chemically defended individuals in a group can confer protection onto conspecifics that had no direct access to clerodanoids, suggesting a 'herd-protection' effect.
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1. The chemical defences of monarch butterflies involve two kinds of secondary plant metabolites: cardiac glycosides (CGs) that are obtained from larval hostplants, and pyrrolizidine alkaloids (PAs) that are gathered by adults usually independent from feeding behaviour. While monarchs and CGs have received great attention, monarchs and PAs appear largely ignored in science as well as by the public. 2. We review and discuss PA-pharmacophagy specifically for Danaus plexippus and its closest relatives and aim to encourage research and future consideration of this peculiar type of insect-plant relationship, which represents an intrinsic but surprisingly understudied aspect of the lives of adult monarchs.
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Danaine butterflies sequester pyrrolizidine alkaloids (PAs) from several plant sources. The underlying mechanisms that mediate this interaction have not been explored. It is also underappreciated whether species that differ in PA demands forage differently. Decision-making in the southern monarch butterfly Danaus erippus (low PA-demand) was compared with the queen butterfly D. gilippus (high PA-demand) in relation to withered and freshly damaged leaves of Crotalaria spectabilis (monocrotaline-rich plant). The ultrastructure of the proboscis and mesothoracic legs of D. erippus, D. gilippus and D. plexippus was also analysed. Attraction of D. erippus and D. gilippus to withered or freshly damaged leaves of C. spectabilis was negligible. The two Danaus species did not scratch leaves and did not differ in feeding time on this PA plant. Butterflies did not visit vegetative PA sources in the field. The proboscis and mesothoracic legs of all Danaus species studied did not present hooks and/or spines for scratching leaves. Basiconic sensilla were found on the surface of the proboscis of all butterfly species analysed. In contrast to the current knowledge on Danaus, these results revealed that common species of the Americas are not attracted to vegetative PA sources. It is suggested that Danaus species may have diversified independently with respect to PA assimilation capacities and use.
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Certain butterflies utilize plant-acquired alkaloids for their own chemical defense and/or for producing male sex pheromone; a trait known as pharmacophagy. Males of the danaine butterfly, Parantica sita, have been reported to ingest pyrrolizidine alkaloids (PAs) as adults to produce two PA-derived sex pheromone components, viz. danaidone (major) and 7R-hydroxydanaidal. We found, however, that not all PAs that can be precursors for the pheromone serve for mating success of males. Here we show that although the sex pheromone is regarded as a requisite for successful mating, uptake of specific PA(s) (lycopsamine-type PAs) is also imperative for the males to achieve copulation. The increase in the levels of two biogenic amines, octopamine and/or serotonin, in the brain and thoracic ganglia of males fed with specific PA(s) suggested that these alkaloids most likely enhance male mating activity. The results can present new evidence for the evolutionary provenance of pharmacophagous acquisition of PAs in PA-adapted insects.
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This book facilitates an integrative understanding of the development, genetics and evolution of butterfly wing patterns. To develop a deep and realistic understanding of the diversity and evolution of butterfly wing patterns, it is essential and necessary to approach the problem from various kinds of key research fields such as “evo-devo,” “eco-devo,” ”developmental genetics,” “ecology and adaptation,” “food plants,” and “theoretical modeling.” The past decade-and-a-half has seen a veritable revolution in our understanding of the development, genetics and evolution of butterfly wing patterns. In addition, studies of how environmental and climatic factors affect the expression of color patterns has led to increasingly deeper understanding of the pervasiveness and underlying mechanisms of phenotypic plasticity. In recognition of the great progress in research on the biology, an international meeting titled “Integrative Approach to Understanding the Diversity of B utterfly Wing Patterns (IABP-2016)” was held at Chubu University, Japan in August 2016. This book consists of selected contributions from the meeting. Authors include main active researchers of new findings of corresponding genes as well as world leaders in both experimental and theoretical approaches to wing color patterns. The book provides excellent case studies for graduate and undergraduate classes in evolution, genetics/genomics, developmental biology, ecology, biochemistry, and also theoretical biology, opening the door to a new era in the integrative approach to the analysis of biological problems. This book is open access under a CC BY 4.0 license.
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A number of butterfly species are toxic or unpalatable against predators by developing mechanisms either to biosynthesize such noxious elements de novo or to acquire directly from the poisonous host plants for their own defense. Most of these “poisonous butterflies” exhibit aposematically colored wing patterns that are often associated either with Batesian or Müllerian mimicry species to form a “mimicry ring.” This review focuses on unpalatable chemical elements potentially operating in three typical mimicry rings: (1) the tiger Danaus mimicry ring, (2) the Idea mimicry ring, and (3) the red-bodied swallowtail mimicry ring, in association with their mimetic wing patterns. Female-limited polymorphisms are a common feature of the Batesian mimicry but not in Müllerian mimicry, because such diversification is unfavorable for the models. I present here some unique cases of sexual dimorphisms within the putative Müllerian mimicry complexes. A Danaus chrysippus-mimicking nymphalid, Argyreus hyperbius, is a typical example of the female-limited dimorphic mimics. However, A. hyperbius were found to be poisonous with toxic cyanogenic glycosides (linamarin and lotaustralin). Likewise, a pipevine swallowtail, Atrophaneura alcinous, which sequesters toxic aristolochic acids, exhibits sexually dimorphic color patterns (male, black; female, smoky brown). A sympatric diurnal zygaenid moth, Histia flabellicornis, is mimetic to A. alcinous males rather than the females and stores cyanogenic glycosides. The moth is regarded as a Müllerian ally that may have stabilized the wing coloration mutually with those of A. alcinous males. On the contrary, a diurnal “swallowtail moth,” Epicopeia hainesii, mimics the brighter wing color of A. alcinous females. Possible adaptation mechanisms on these paradoxical mimicry patterns are discussed.
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Context: The genus Premna (Lamiaceae), distributed throughout tropical and subtropical Asia, Africa, Australia and the Pacific Islands, is used in folk medicine primarily to treat inflammation, immune-related diseases, stomach disorders, wound healing, and skin diseases. Objectives: This review exhaustively gathers available information on ethnopharmacological uses, phytochemistry, and bioactivity studies on more than 20 species of Premna and critically analyzes the reports to provide the perspectives and directions for future research for the plants as potential source of drug leads and pharmaceutical agents. Methods: A literature search was performed on Premna species based on books of herbal medicine, major scientific databases including Chemical Abstract, Pubmed, SciFinder, Springerlink, Science Direct, Scopus, the Web of Science, Google Scholar, and ethnobotanical databases. Results: More than 250 compounds have been isolated and identified from Premna species, comprising of diterpenoids, iridoid glycosides, and flavonoids as the most common secondary metabolites, followed by sesquiterpenes, lignans, phenylethanoids, megastigmanes, glyceroglycolipids, and ceramides. Many in vitro and in vivo studies have been conducted to evaluate the biological and pharmacological properties of the extracts, and isolated compounds of Premna species with antimicrobial, antioxidant, anti-inflammatory, immunomodulatory, antihyperglycaemia, and cytotoxic activities. Conclusion: The bioactive compounds responsible for the bioactivities of most plants have not been well identified as the reported in vivo pharmacological studies were mostly carried out on the crude extracts. The isolated bioactive components should also be further subjected to more preclinical studies and elaborate toxicity study before clinical trials can be pursued.
In recent decades, a burgeoning literature has documented the cultural transmission of behavior through social learning in numerous vertebrate and invertebrate species. One meaning of “cultural evolution in animals” refers to these discoveries, and I present an overview of key findings. I then address the other meaning of the term focused on cultural changes within a lineage. Such changes in humans, described as “cumulative cultural evolution,” have been spectacular, but relatively little attention has yet been paid to the topic in nonhuman animals, other than asserting that the process is unique to humans. A variety of evidence including both controlled experiments and field observations has begun to challenge this view, and in some behavioral domains, notably birdsong, cultural evolution has been studied for many years. In this review, I dissect concepts of cultural evolution and cumulative culture and appraise the accumulating evidence bearing on their nature and significance for evolutionary biology at large. Expected final online publication date for the Annual Review of Ecology, Evolution, and Systematics Volume 50 is November 4, 2019. Please see for revised estimates.
Species co-occurrence in ecological communities is thought to be influenced by multiple ecological and evolutionary processes, especially colonization and competition. However, effects of other interspecific interactions and evolutionary relationships are less explored. We examined evolutionary histories of community members and roles of mutualistic and parasitic interactions (Müllerian and Batesian mimicry, respectively) in the assembly of mimetic butterfly communities called mimicry rings in tropical forests of the Western Ghats, India. We found that Müllerian mimics were phylogenetically clustered, sharing aposematic signals due to common ancestry. On the other hand, Batesian mimics joined mimicry rings through convergent evolution and random phylogenetic assembly. Since the Western Ghats are a habitat island, we compared species diversity and composition in its mimicry rings with those of habitat mainland to test effects of biogeographic connectivity. The Western Ghats consisted of fewer mimicry rings and an overall smaller number of aposematic species and mimics compared to habitat mainland. The depauperate mimicry rings in the Western Ghats could have resulted from stochastic processes, reflecting their long temporal and spatial isolation and trickling colonization by the mimetic butterfly communities. These results highlight how evolutionary history, biogeographic isolation, and stochastic colonization influence the evolutionary assembly and diversity of ecological communities.
Close associations of certain lepidopteran taxa with pyrrolizidine alkaloids (PAs), a typical class of plant secondary metabolites, have been well documented from the perspective of evolutionary ecology. Male danaine butterflies are thought to utilize PAs as precursors for the production of dihydropyrrolizines [e.g. danaidone (DO) and hydroxydanaidal (HD)] in their two distinct androconial organs, viz. alar scent organs (sex brands) and abdominal hairpencils. However, little is known about the quantitative profiles of these compounds in danaines, the mechanism for their formation in the androconial organs, or their biological functions, particularly in mating behaviour. The present study addressed these unanswered questions posed for males of the danaine butterfly, Parantica sita. Chemical analyses of androconial extracts revealed considerable seasonal/regional and individual variations of the amounts of DO (the major dihydropyrrolizine produced) and 7R-HD (the 7R-enantiomer of HD detected in this study) found in the two organs. These variations seemed to depend primarily on the age of the male and the phenological traits of PA-containing plants available. Males were found to acquire an adequate capability to produce DO ~1 week after eclosion. DO was shown to be produced exclusively in the sex brand and subsequently physically transferred to the hairpencil through a contact behaviour between the two organs, here termed ‘perfuming behaviour’. The results of behavioural experiments with PA-fed and PA-unfed males that were allowed to compete for mates, combined with the positive electroantennographic (EAG) responses of the female, to both DO and 7R-HD, led to the conclusion that either or both of these compounds can act as the sex pheromone. Oral administration of PAs to males indicated that DO can be biosynthesized from various PA precursors, while 7R-HD, unlike in arctiid moths, is derived only from PAs with the 7R-configuration. The putative biosynthetic pathways of DO and 7R-HD, and the evolutionary provenance of the binate androconial system in the Danainae are also discussed.