Ancient butterfly ﾑ antsymbiosis: direct evidence from
Dominican amber
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SUMMARY
Although symbioticassociation with ants is pervasivein the butterflyfamiliesLycaenidae and Riodinidae
the age
of these symbioses has never
been estimated
explicitly.
Here we report the first known fossil
ri0.dinidcaterpillar.This fossil can be dated minimally between 15 and 20 Ma old, and confidently
placed in the extant genus Theope.Differing little from modern day Theope,this fossil from Dominican
amber provides direct evidence that secretory and acoustical organs used by modern caterpillars to
mediate symbioses with ants have been highly developed at least since the Miocene. This fossil therefore
becomes the point of referencefor future studiesusing molecular clockmethodsfor dating thesesymbioses
within the riodinid butterflies.
Modern evidence, and the abundance of dolichoderine ants in Dominican
amber (nowextinctin theWestIndies) imply that specialized symbioticrelationshipsbetween Theopecater-
pillars and these ants were likely in existence at least 15 Ma ag0. The current distribution of neotropical
riodinid butterfly and ant faunas indicates the extinction in the West Indies of at least two unrelated taxa
that formed a tightly linked symbiotic association, which persisted to the present elsewhere
1. INTRODUCTION
ﾑ
Among butterflies the ability to form intimate associaﾂ
tions with ants has evolved only in the lycaenoids the
families Lycaenidae and Riodinidae (Cottrell 1984;
Pierce 1987;DeVries 1991a,1997;Fiedler 1991).The
fundamentalnature of these symbioticassociations is
that caterpillars provide ants with food secretionsin
exchange for protection against predators (Cottrel1
1984;Pierce 1987;Pierceet a1.1987;DeVries 1988,1997;
DeVries & Baker 1989).Experimental studieson both
groups have demonstratedthat when they are found
by insect predators and parasitoids, caterpillars
without ant
symbionts have little chance of surviva1,
whereas caterpillars with ant symbionts are provided
significant protection against these natural enemies
(e.g. Pierce & Mead 1981;Pierce et a1. 1987;DeVries
1991&;Cushmanet a1. 1994).By virtue of the strong
influence
fitness the maintenance of a
is at a premium, and this is
achieved through the use of specialized secretory
organs that not only produce food secretionsto ants,
but may also produce semiochemicalsthat modify ant
constant
on caterpillar
guard of ants
behaviours (Cottrell 1984;DeVries 1988, 199k, 1997;
Fiedler & Suefert1996).
Vibrational communication
is prevalent among
ants
(Holldobler & Wilson 1990),and studiessuggest that
these signals
are
used by some ants as part of colony
substrate-borne acoustical
is a widespread trait
these calls bear similarities to ant vibrational signals
(DeVrieset a1.1993;DeVries,unpublisheddata). Thus,
1ycaenidand riodinid caterpillar calls are considered
to function in concert with
secretory organs
to achieve
and maintain ant symbionts (DeVries1990, 199k, 1997;
DeVries et a1. 1993). Although the mechanisms for cater ﾂ
pillar call production in all lycaenidsand membersof
the riodinid tribe Eurybiini remain unknown, it has
been demonstrated that riodinid caterpillars in the
tribes Lemoniini and Nymphidiini produce calls by
using paired organs, termed vibratory papillae
(DeVries1990,1991c,1997).
Despite the prevalence of riodinid caterpillars in
the tribes Eurybiini, Lemoniini and Nymphidiini to
form intimate associationswith ants (Harvey 1987;
DeVries 1997;DeVries et a1. 1994), the age of these
symbioticinteractionsis unknown.The origin of ri0dinid-ant
associations
could potentially be estimated
indirectlyusing molecular clock methodswith a phy1ogenetichypothesis(Kimura 1983;Li & Graur 1991),
0r directly through the fossil record. However, the
ofmolecular
this phenomenon
has and
never been estimated by
ck
Od
山
exis
dence
1137
calls
lycaenid and riodinid caterpillars that form
symbioses with ants (DeVries, 1990, 199k), and that
among
age
*Author for correspondence,
Proc. R. Soc. Lond. B (1997) 264, 1137-1140
Printed in Great Britain
communication
and recruitment (Marki & Holldobler
1978;Baroni-Urbaniet a1.1988;Roces et a1.1995).It has
recently been established that the ability to produce
日
S
@
no P
en
卜
ev
ｩ 1997 The Royal Society
1138 P.J. DeVries and G. 0. Poinar Ancient
butterfly-ant
symbiosis
Dominican
portant
to our
amber fossils have been extremely im ﾂ
understanding of insect evolution and
biogeography (e.g. Baroni-Urbani 1980; Wilson
1985a,&;Poinar 1992,1996;Grimaldi 1991,1996a),but
fossil inclusions of butterflies in Dominican amber are
exceedingly rare. Three adult butterflies of the same
species are known from Dominican amber, all of which
possess systematic affinities with the mainland neotr0pical genus Mipaea, but not to the only extant West
report thereforeprovidesthe first direct evidencethat
secretory and acoustical organs used by riodinid butter ﾂ
fly caterpillars to mediate symbioses with ants were
highly developed at least 15ﾑ 20 Ma ag0, and serves to
constrain future studies that approximate the age of
riodinid-ant symbioses using a molecular clock.
There are currently about 50 species in the genus
Theope,with members occurring in lowland forests
throughout Mexic0, Central and South America, and
Indian riodinid,Dianesiacarteri(Harvey 1987;Grima1- on Trinidad and Tobago (Seitz 1916-1920;Barcant
di 1996a;DeVries 1997).As neitherpresent day Napaea 1970;Harvey 1987;Bridges 1988),but they are absent
caterpillars and its relatives, or caterpillars of Dianesia
and its close relatives possess specialized organs to form
associationswith ants (seesummariesin Harvey 1987;
DeVries 1997),riodinid-ant symbioses
from the West Indies.
Here
are
unknown
the first fossil rio ﾂ
dinid caterpillar in Dominican amber that not only
providesthe first accurate benchmarkfor dating the
antiquity of riodinid ﾑ ant symbioses, but it contributes
further evidence for the historical extinction of major
we report
of fauna in the DominicanRepublic.
groups
2. RESULTS
AND
ranges
1997), therefore establishes the extinction of at least two
riodinid taxa from the West Indies.
Two points suggest that the palaeoriodinid fauna of
the West Indies included more than two taxa. First, it
entomofauna was similar to the composition ofentom0-
The unique amber piece containing the riodinid ca ﾂ
the northern mountain
reportedhere, togetherwith the other Dominican amber fossilriodinid species(seeGrimaldi 1996fl;DeVries
is likely that the compositionof the Domincanpalae0-
DISCUSSION
terpillar originatedfrom the Lalbca
from the West Indies. The contemporary West Indian
riodinid fauna consists of a single species, Dianesia carten, and this taxon is confined entirely to Cuba and the
Bahamas (Spencer-Smith et a1. 1994). The fossil Theope
group
of mines in
of the Dominican
Re ﾂ
public located in the El Mamey Formation (Upper
Eocene), which is composed of shale-sandstone inter
ﾂ
spersedwith a conglomerateof wel1-roundedpebbles
(Eberle et a1. 1980). Recent biostratigraphicand pa1aeostratigraphic evidence indicates that all
Dominican amber was formed in a single sedimentary
basin dated from 15ﾑ 20 Ma old (Iturralde-Vincent &
faunas found presentlyin Central and South America
(Baroni-Urbani & Saunders 1980; Wilson 1985a,A).
Analyses of 11 contemporary Central and South
American riodinid faunas indicate that approximately
30% of the total species richness at each site is ac ﾂ
counted for by taxa
that form symbioses with ants
(see DeVries 1997). Based on these estimates the Domin ﾂ
ican palae0-riodinid fauna would be predicted to
include a minimum of three to four species. Second,
the palae0-entomofauna
in Dominican amber remains
largely unstudied, and future work will undoubtedly
MacPhee1996),whereas previous chemical and fossil
increase the number of taxa
old (Schlee1990).
like riodinid butterflies. Therefore both comparative estimates based on present day faunas, and the
quantity of Dominican amber material yet to be exammned，， uggeSt 、 I。ぬ P、 l" 0- I"dinid 伍una than
evidence has suggested an age of 30-40 million years
The combined presence of tentacle nectary organs,
vibratory papillae, and bal100n setae are found only on
riodinid caterpillars in the tribe Nymphidiini, and no ﾂ
where else among the Lepidoptera (Gottrell 1984;
Harvey 1987;DeVries 1997).Thus, the possessionof all
three of thesespecialized organs by this fossil (figure 1)
place it unquestionably
as a
riodinid
caterpillar
that
formed symbioses with ants. Possessionof exaggerated
bal100n setae along the anterior margin of the first
thoracicsegment is typical of caterpillarsin the genus
Theope,although less exaggerated bal100n setae are
found in the close relative Nymphidwm(Harvey 1987;
DeVries 1997).Present day Theope caterpillars possess
strongly developed ventr0-1ateralflanges on all body
segments, long plumose lateral body setae, and absence
above what is currently
known(Poinar 1992,unpublisheddata), includingrare
taxa
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A wide range of fossil evidence indicates that ancient
symbioticassociationshave been remarkably persistent
through evolutionary time (reviewedin Boucot 1990;
Poinar 1992).For example, Wasmann(1932)described
a reduviid bug with
its Dolichoderus ant prey from Baltic
amber, and noted that it differed little from modern
day ancestors who remain apparent specialists on these
same ants. Other examples are found in Dominican
amber (Poinar 1992),and one of the most spectacular
is an alate Acropyga. ant queen carrying a symbiotic scale
insect in her mandibles (Grimaldi 1996&).Excepting
the single record of Theopeguillaumeibeing tended by
ants (while feeding on the Azteca-mhabhed
Nymphidiumcaterpillars (Penz & DeVries,unpublished Solenopsis
ant-plant Cecropid),
all other observations indicatethat
data). A detailed comparison on contemporary
cater ﾂ
pillars of four speciesof Theope (T. matuta, T. guillaumei, present day Theope caterpillarstypically form obligate
T. virgilius,T lycaenma),
and four Nymphidiumspecies(AC symbioses with dolichoderine ants, especially the gen ﾂ
era Azteca and Dolichoderus (DeVries et a1. 1994; DeVries
mantus, M. balbinus,.ACnr baeotia,.ACcachrus},
not only
1997,unpublisheddata). In theseobligatesymbioses the
showedthat the fossilmay be confidently placed in the
exaggerated bal100n setae surrounding the head of
genus Theope (probablyin the fourth, and penultimate
instar), but that it falls within the overall variation ob ﾂ
Theopecaterpillars(figure 1) appear important in medﾂ
served among different speciesof present day Theope iating associationswith dolichoderine ants by providing
semiochemicalstimuli to ant symbionts (DeVries1997).
caterpillars (see illustrations in DeVries (1997)).This
of anterior tentacle organs, traits that are not shared by
・
・
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Ap
L
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Figure 1. Fossil Theopecaterpillar in Dominican amber, (a) Photographof the fossil in dorsal view. (A) Illustration of the entire
caterpillars that form symbioses with ants: conspicuouscorona of
bal100n setae on thoracic segment one, the wel1-developed anal plate (Ap) on abdominalsegments nine and ten, and the external
orifices of the tentacle nectary organs (tno) on abdominal segment eight, (c) Illustration of head and first thoracic segment
detailing the placement of vibratory papillae (Vp) on anterior edge ofthoracic segment one. The vibratory papillae function in
the production of substrate borne acoustical signals that enhancemodernriodinid caterpillar-ant symbioses.
fossil in dorsal view showing features characteristic ofriodinid
Proc. R. Soc. Land. B (1997)
1140 P.J. DcVries and G. 0. Poinar Ancient
butterfly-ant
symbiosis
of A^teca and Dolichoderus ants
in Do
ﾂ
minican amber (Wilson ¥985a,b) suggests that a
specialized relationship between Theopeand these dolichoderine ants is likely
Ma
Moreover,
ag0.
to have
existed at least 15-20
is the case for Theopebutterflies,
as
neither Azteca or Dolichoderus are part of the living Do ﾂ
minican Republic ant fauna, but these ant genera form
principalelements of mainlandneotropical foresthabitats (Wilson 1985a;Holldobler & Wilson 1990).Thus,
0ur report not only provides evidence for the extinction
of Theopefrom the Dominican Republic,but points to
the possible correlated extinctions of two unrelated spe ﾂ
cies that acquired, and maintained a tightly linked
symbiotic association that has survived to the present
in Central and South America.
WC are grateful to C. M. Penz for illustrating the fossi1, and
comparingTheopeand JVymphidiumcaterpillars. WL also thank
J. King-Koyne, D. Drift, D. Grimaldi, R. Lande, M. Lynch,
C. M. Penz, T. Walla, and two
anonymous
reviewers for
pro ﾂ
viding valuable comments on the manuscript. The Dominican
amberfossil is in the Poinar ambercollection at Oregon State
University, Corvallis, Oregon. This research was funded in
part by aJ. S. GuggenheimFellowship to P. J. DeVries, and is
dedicated to the acoustical research of the late T.Williams.
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勿 r坤比川J 川口9収
in 山ee West
Dominican
The
amber
subfamily