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A Mosaic of Chemical Coevolution in a Large Blue
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Carnegie Institution of Washington, and the Woods Hole
Supporting Online Material
Figs. S1 and S2
26 July 2007; accepted 27 November 2007
A Mosaic of Chemical Coevolution in a
Large Blue Butterfly
David R. Nash,1* Thomas D. Als,2† Roland Maile,3‡ Graeme R. Jones,3Jacobus J. Boomsma1
Mechanisms of recognition are essential to the evolution of mutualistic and parasitic interactions
between species. One such example is the larval mimicry that Maculinea butterfly caterpillars use to
parasitize Myrmica ant colonies. We found that the greater the match between the surface chemistry of
Maculinea alcon and two of its host Myrmica species, the more easily ant colonies were exploited. The
geographic patterns of surface chemistry indicate an ongoing coevolutionary arms race between the
butterflies and Myrmica rubra, which has significant genetic differentiation between populations, but
not between the butterflies and a second, sympatric host, Myrmica ruginodis, which has panmictic
populations. Alternative hosts may therefore provide an evolutionary refuge for a parasite during
periods of counteradaptation by their preferred hosts.
of host populations, so that selection for costly
defensive discrimination between kin and para-
sites by the host (2, 3) may be weak (4). This
parasitize multiple host species (5–7). However,
whenparasites are common enough, selection on
hosts to avoid being parasitized fuels coevolu-
tionary arms races, in which parasites evolve
better mimicry and hosts improve their recog-
nition of parasites (8, 9).
The dynamics of parasite density and distri-
bution can be explained by geographic mosaic
ocial and brood parasites often use mimic-
ry to exploit their hosts (1, 2). These
models of coevolution (10), which allow differ-
local populations. In these models, mutual coad-
interactions (hotspots), whereas parasites and
hosts may evolve independently in other pop-
ulations (coldspots). Theoretical studies have ex-
plored geographic mosaic models (11, 12), but
there have been few empirical tests of ecological
systems in which the mechanisms of coevolution
and the patterns of interaction were known (10).
The Alcon blue butterfly, Maculinea alcon,is
socially parasitic on two species of Myrmica ants
in Denmark (13). The butterfly’s caterpillars ini-
tially develop on marsh gentian plants, Gentiana
by a foraging Myrmica worker (Fig. 1B). Once
inside the host ant nest, caterpillars are fed by the
ants in preference to their own larvae (14), re-
ducing host fitness, particularly in small colonies
(15) (Fig. 1C and fig. S2). The overlap in dis-
tribution of the widespread host ants and the rare
host plant is small, both locally and regionally,
and there is geographic variation in the abun-
dance and use of the two host ant species (13).
Populations of the Alcon blue are therefore
patchy, and only a small fraction of host ant
populations are parasitized and potentially sub-
ject to selection for resistance. The parasite is
absent from most host populations, which are
therefore coevolutionary coldspots (10, 11). In
much of Europe, a third ant species, Myrmica
scabrinodis, is also a host of the Alcon blue (16),
but infection of this species has never been
observed in Denmark, despite its abundance on
Danish M. alcon sites (13).
1Institute of Biology, University of Copenhagen, Universitet-
sparken 15, DK-2100Copenhagen, Denmark.2Department of
Genetics and Ecology, University of Aarhus, DK-8000 Å rhus C,
Staffordshire ST5 5BG, UK.
*To whom correspondence should be addressed. E-mail:
†Present address: Population Genetics Laboratory, Danish
Institute for Fisheries Research, Vejlsoevej 39, DK-8600
‡Present address: Trivadis GmbH, D-70565 Stuttgart, Germany.
3School of Chemistry, Keele University, Keele,
Number of Maculinea alcon caterpillars in nest
Proportion of nests with brood
Fig. 1. Effect of the parasitic Alcon blue butterfly on its host ant colonies. (A)
Caterpillar emerging from a G. pneumonanthe bud with eggs. (B) Recently emerged
caterpillar being carried to the nest by a worker of M. rubra. [Photographs, D. R. Nash]
(C) Relationship between the number of caterpillars present in small, medium, and
large M. rubra nests (SOM text) in late spring and the probability of ant brood being present. The area of each symbol is proportional to the number of
nests observed with that number of caterpillars. Lines are fitted logistic regressions.
4 JANUARY 2008VOL 319
on April 29, 2008
Alcon blue caterpillars were adopted more
rapidly by host ants from the populations that
they infect than by the alternative host species
present in the same area (sympatric). However,
local parasite maladaptation (host resistance)
of caterpillars was by Myrmica rubra colonies
tion time is a good measure of infectivity of the
parasite that combines the speed of retrieval of
caterpillars and initial integration into the ant
Maculinea caterpillars are thought to infect
Myrmica nests by mimicking the surface chem-
istry of the ant brood (19, 20). We collected sam-
ples of pre-adoption parasite caterpillars and host
ant larvae from the same three populations that
were previously used for the cross-infection ex-
(15, 17). Qualitatively, the caterpillars of M. alcon
shared the same set of surface compounds,
whereas the nonhost ant M. scabrinodis did
not (Fig. 2A, fig. S1, and table S1). Quantita-
tively, however, the relative abundances of the
M. alcon (Fig. 2B) and its two ant hosts (figs. S1
and S3). Chemical similarity was a significant
predictor of infectivity, explaining 62% of the
variation in adoption time for M. rubra and
78% for M. ruginodis (Fig. 2, C and D).
Local selection on hosts should favor herita-
ble [Supporting Online Material (SOM) text]
changes in ant larval surface chemistry if this al-
lows discrimination between ants and Maculinea
caterpillars (21). Because the patchy Maculinea
populations are expected to counter host resist-
ance, coevolutionary hotspots are created. There-
are in a coevolutionary arms race in degree of
hydrocarbon profile matching and that there are
different trajectories in change in surface chem-
istry between hotspots. However, if substantial
lations and nearby uninfected subpopulations,
any parasite-induced selection on the ants to
change recognition compounds is likely to be
ineffective, resulting in a coevolutionary cold-
spot. Previous work suggested that M. rubra has
levels of gene flow much lower than those of
M. ruginodis (22).
We compared the surface chemistry of ant
larvae from uninfected nests of M. rubra and
M. ruginodis from the three sites with M. alcon
and from three sites where the butterfly has
never been recorded (15) (Fig. 3A). The chem-
ical profiles of M. rubra (Fig. 3B) differed
significantly between the six populations (Wilk’s
l10,40= 0.159, P < 0.0001) because of divergent
between uninfected populations (l4,20= 0.899,
not have significantly different surface chemical
profiles between populations (l10,48= 0.612, P=
0.414), and differences between infected pop-
ulations (l4,22 = 0.960, P = 0.976) were no
greater than those between uninfected popula-
tions (l4,24= 0.852, P = 0.735).
genetic differentiation between populations, by
using three variable microsatellite loci (15) to
examine whether differences in chemical profiles
between and among parasitized M. rubra and
ulations of M. rubra were strongly genetically
differentiated, with anoverallFSTof0.136[P<
values (table S3)], whereas populations of
M. ruginodis were not (FST= 0.004, P = 0.473).
Our FSTestimate for M. rubra over distances
over a few hundred meters, confirming that this
species has highly viscous populations with little
local gene flow. We also measured Wright’s FIS,
for the two ant species, with M. ruginodis [FIS=
0.187 (table S4)] being somewhat more inbred
than M. rubra (FIS= 0.136). Thus, inbreeding is
not associated with the higher hydrocarbon
The corresponding values for M. alcon were
FST= 0.182 and FIS= 0.132, estimates very sim-
all three species have patchy populations but that
migration is higher in M. ruginodis than in either
M. rubra or M. alcon.
We found a relatively constant infection rate
for M. ruginodis nests (range of 8 to 40%) across
all sampled populations (13), whereas infection
ratesof M.rubranestsvaried from 0to72%.For
M. rubra, the infection rate increased with the
prevalence of M. rubra (logistic regression, r2=
40.86, d.f. = 5, P < 0.0001), whereas no such
relationship existed for M. ruginodis (r2= 4.59,
d.f. = 7, P = 0.71). This is consistent with the
but not to M. ruginodis as host populations
The changes in host surface chemistry in
parasitized M.rubra populationsindicate that the
M. alcon–M. rubra combination forms a geo-
graphic mosaic of coevolutionary hotspots, with
a continuing arms race in chemical mimicry,
whereas the sympatric M. alcon–M. ruginodis
interaction does not. An alternative interpreta-
tion, that the changes in hydrocarbon profiles
of M. rubra reflect environmental differences
between infected and uninfected sites, seems un-
gences and the lack of divergence in uninfected
populations. If anything, we expect uninfected
populations to be more environmentally variable
than infected populations because they occur in a
range of habitats, whereas infected populations
Fig. 2. Chemical mimicry of Myrmica ants by Alcon blue caterpillars. (A)
Representative gas chromatograms for surface extracts of caterpillars of
M. alcon, larvae of the host ants M. rubra and M. ruginodis, and larvae of the
sympatric nonhost M. scabrinodis. (B) Ordination plots showing the first two
three sample sites. Markers show the chemical profiles for individual
caterpillars. The data for each study population are enclosed by a minimum
Adoption time (min)
convex polygon. (C and D) Relationship between adoption time (log scale)
and dissimilarity in chemical profiles (Mahalanobis distance) between
M. alcon caterpillars and larvae of M. rubra (C) and M. ruginodis (D). Each
point is the mean ± SE of five observations for each of the nine combinations
of butterflies and ants from the three infected sites (17). Lines are major axis
regressions: for M. rubra, r2= 0.62, P = 0.011; for M. ruginodis, r2= 0.78,
P = 0.002.
VOL 3194 JANUARY 2008
on April 29, 2008
must overlap the niche of G. pneumonanthe.
Lack of profile variation between uninfected
populations has previously been demonstrated
for M. rubra over much larger distances (20).
The within-population variation in cuticular
hydrocarbon profiles was consistently higher
in infected populations than in uninfected
populations of M. rubra (sum multivariate test;
F1,4= 10.56, P = 0.034) but not M. ruginodis
(F1,4= 0.17, P = 0.455), which further supports
M. alcon is a virulent parasite of Myrmica
ants (Fig. 1C and SOM text) that will reduce the
size and density of host colonies. This, coupled
with the density-dependent infection rate for one
dynamic shifts in host use over time. Although
M. rubra is not a host at site A (13), we observed
strong divergence in its chemical profiles at this
site (Fig. 3B), which may reflect former use of
this host. The coevolutionary coldspots provided
by M. ruginodis may thus allow M. alcon to
M. rubra (SOM text), but this may also put an
ultimate limit on how far M. alcon can diverge
from the relatively static chemical profile of
similar to each other chemically (20), so it is
unlikely that such a system could exist for
parasites that use more distinct hosts.
Our findings are consistent with geographic
mosaic models for coevolution (24) and confirm
that restricted gene flow is a crucial prerequisite
for local coevolution (25). Our results also have
Alcon blue, which is increasingly threatened
throughout much of its range (26). Other
Maculinea species have been reintroduced to
areas where native species have gone extinct
without prior screening of similarity in genetics
or cuticular chemical profiles (27, 28). Our data
suggest that this is reasonable for Maculinea
species that rely on relatively panmictic species
of Myrmica host ants because successful reintro-
ductions can likely be made from any source
population that uses the same host ant. However,
for Maculinea species that rely on genetically
differentiated host ants, the match between the
cuticular chemical profiles of caterpillars and ant
larvae should be carefully considered.
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H. Jungnickel, and J. Tentschert for chemical analysis; and
J. Frydenberg, J. Ebsen, and A. Lomborg for microsatellite
analysis. D.R.N. was supported by European Union (EU)
Marie Curie and Carlsberg Foundation fellowships.
Collaboration between Denmark and Keele was via the EU
research training networks Social Evolution, which
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Insect Societies (INSECTS). Population genetic analysis of
M. alcon was supported by the EU Research Training and
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study were supported by the Danish National Research
Foundation (J.J.B. and D.R.N.).
Supporting Online Material
Materials and Methods
Figs. S1 to S3
Tables S1 to S4
14 August 2007; accepted 26 November 2007
Prevalence of host
Fig. 3. Adaptation of Myrmica host ants to infection by Alcon blue caterpillars. (A) The current (after
and Z) populations are marked. (B and C) Ordination plots showing the first two principal components of
the chemical profilesofM.rubra (B) and M.ruginodis(C).Colored markersshowthe chemicalprofilesfor
individual nests, and the data for each study population are enclosed by a minimum convex polygon. The
centroid of each population (black dot) is labeled and linked by a line to the overall centroid of the three
prevalence (proportion of the totalhost nests that are of that species) for the two host ant species present
in each of seven populations of M. alcon examined in Denmark (13). Lines are fitted logistic regressions.
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