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Climatic Gradients of Arms Race Coevolution.

Author(s): Hirokazu Toju, Harue Abe, Saneyoshi Ueno, Yoshiyuki Miyazawa, Fumiya Taniguchi,
Teiji Sota, and Tetsukazu Yahara
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Source: The American Naturalist, Vol. 177, No. 5 (May 2011), pp. 562-573
Published by: The University of Chicago Press for The American Society of Naturalists
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vol. 177, no. 5 the american naturalist may 2011
Climatic Gradients of Arms Race Coevolution
Hirokazu Toju,
1,2,
* Harue Abe,
3
Saneyoshi Ueno,
4
Yoshiyuki Miyazawa,
5
Fumiya Taniguchi,
6
Teiji Sota,
1
and Tetsukazu Yahara
7
1. Graduate School of Science, Kyoto University, Sakyo, Kyoto 606-8502, Japan; 2. Hakubi Center, Kyoto University, Sakyo, Kyoto 606-
8501, Japan; 3. Graduate School of Agricultural Science, Tohoku University, Miyagi 989-6711, Japan; 4. Forestry and Forest Products
Research Institute, Ibaraki 305-8687, Japan; 5. University Forest of Kyushu, Kyushu University, Fukuoka 811-2415, Japan; 6. National
Institute of Vegetable and Tea Science, Kagoshima 898-0087, Japan; 7. Faculty of Sciences, Kyushu University, Fukuoka 812-8581, Japan
Submitted July 5, 2010; Accepted December 28, 2010; Electronically published April 8, 2011
Online enhancement: appendix. Dryad data: http://dx.doi.org/10.5061/dryad.8186.
abstract: In nature, spatiotemporally dynamic coevolutionary pro-
cesses play major roles in the foundation and maintenance of bio-
diversity. Here, we examined the arms race coevolution involving a
seed-eating weevil with a long snout and its camellia plant host with
a thick fruit coat (pericarp) throughout the marked climatic gradient
observed across the Japanese islands. Results demonstrated that fe-
male weevils, which bored holes through camellia pericarps to lay
eggs into seeds, had evolved much longer snouts than males, espe-
cially in areas in which Japanese camellia pericarps were very thick.
The thickness of the plant pericarp was heritable, and the camellia
plant evolved a signicantly thicker pericarp on islands with the
weevil than on islands without it. Across populations with weevils,
resource allocation to plant defense increased with increasing annual
mean temperature or annual precipitation, thereby geographically
differentiating the evolutionary and ecological interactions between
the two species. Given that the coevolutionary relationship exhibited
appreciable variation across a relatively small range of annual mean
temperatures, ongoing global climatic change can dramatically alter
the coevolutionary process, thereby changing the ecological inter-
action between these species.
Keywords: arms race, climate change, coevolution, host-parasite,
prey-predator, productivity gradient.
Introduction
One of the major challenges in science is to understand
how anthropogenic changes in the global environment al-
ter coevolving networks of biological communities
(Thompson 2005; Benkman et al. 2007). Researchers have
recently acknowledged that global climate change rapidly
alters the ecological processes of plant-pollinator (Hegland
et al. 2009), plant-herbivore (van Asch and Visser 2006),
host-parasite (Brooks and Hoberg 2007), and prey-pred-
ator (Durant et al. 2007) systems by causing phenological
* Corresponding author; e-mail: toju@terra.zool.kyoto-u.ac.jp.
Am. Nat. 2011. Vol. 177, pp. 562573. 2011 by The University of Chicago.
0003-0147/2011/17705-52288$15.00. All rights reserved.
DOI: 10.1086/659624
and geographical range mismatches between partner spe-
cies or by altering energy ow through trophic levels (Par-
mesan 2006; Tylianakis et al. 2008). Another recent con-
ceptual advance is the recognition that environmental
change can alter the form and strength of natural selection
on traits mediating interspecic interactions within short
time periods, for example, during several or fewer decades
(Grant and Grant 2002; see also Thompson 1998; Kinnison
and Hendry 2001; Carroll et al. 2007). These rapid evo-
lutionary changes are expected to alter the population dy-
namics of interacting species (Yoshida et al. 2003; Hairston
et al. 2005; terHorst et al. 2010), the intensity of ecological
interactions (Carroll et al. 2005), and the composition of
local communities (Whitham et al. 2006). Nonetheless,
few studies have integrated investigations of reciprocal
adaptive processes and knowledge of the potential impacts
of climate change on ecological processes. Accordingly, to
further understand how biological communities will re-
spond to ongoing climate change, environmental depen-
dence of coevolutionary dynamics should be intensively
investigated.
Recent coevolutionary studies have shown that recip-
rocal adaptive processes of interacting species are dynam-
ical in space and time due to various mechanisms and
factors such as local community structure or spatiotem-
porally varying ecological conditions (Thompson 1999,
2005, 2009). In a variety of interspecic systems, traits
mediating coevolutionary interactions vary across popu-
lations (Benkman 1999; Brodie et al. 2002; Zangerl and
Berenbaum 2003; Toju and Sota 2006a, 2006b), and the
processes underlying the diversication of the coevolving
traits are attributed to geographic selection mosaics (Sie-
pielaki and Benkman 2004; Toju 2007), in which the
genotype-by-genotype evolutionary interactions between
species differ among local environments ( in- G #G #E
teractions; Thompson 2005, 2009). Likewise, environmen-
tal conditions potentially determine the intensity of eco-
logical interactions between species (e.g., predation or
Climatic Gradients of Coevolution 563
parasitization rate), thereby inuencing the direction and
strength of local coevolutionary selection (Forde et al.
2004; Lopez-Pascua et al. 2010). For example, in host-
parasite interactions, high growth rates of host populations
(i.e., high productivity) can entail the rapid increase of
parasites and the resulting severe parasitization pressure
can promote the evolution of host defense and the coun-
terevolution of parasite offense (Hochberg and van Baalen
1998; Sasaki and Godfray 1999). Therefore, if the birth
rates of a host species are determined by local environ-
mental conditions, ecological and evolutionary interac-
tions with its parasite would be differentiated among pop-
ulations (Forde et al. 2004; Lopez-Pascua et al. 2010).
Thus, the snapshots of the curent spatial mosaics of
coevolutionary interactions provide valuable opportunities
for inferring the potential effects of climatic environments
on the ecological and evolutionary processes of interspe-
cic interactions in nature.
An ideal system for elucidating the environmental de-
pendence of coevolutionary processes can be observed in
the geographically structured interaction involving a weevil
with an extremely long drill and its host plant featuring
a thick defensive wall (Toju and Sota 2006a, 2006b, 2009;
Toju 2007). Females of the camellia weevil (Curculio ca-
melliae; Coleoptera: Curculionidae) use their snouts to
bore through the thick pericarp of the fruit of the Japanese
camellia (Camellia japonica; Theaceae) and deposit their
eggs into the camellia seeds using long ovipositors (g.
1A1G). Our previous study showed that the longer the
snouts of the weevil, the more likely the boreholes will
reach seeds, whereas the thicker the camellia pericarps, the
more likely the plant will successfully protect its seeds
(Toju and Sota 2006b). The observed geographic corre-
lation between the snout length of female weevils and
camellia pericarp thickness across populations (Toju and
Sota 2006a, 2006b; Toju 2008) suggested that at least each
species has locally adapted to the other and the entire area
of these interactions represents a geographic mosaic of
coevolution (Brodie et al. 2002; Thompson 2005; Beren-
baum and Zangerl 2006; Thompson and Fernandez 2006).
Our previous studies have further shown that the extent
of the weevil-camellia arms race varied along latitudinal
and altitudinal gradients (Toju and Sota 2006b; Toju 2008,
2009), suggesting that some kinds of climatic factors are
responsible for the geographic differentiation of the co-
evolutionary processes.
Here, we conduct a comprehensive survey of climatic
factors organizing the spatiotemporally dynamic process
of the weevil-camellia coevolution. The aim of this study
is fourfold. First, by focusing on sexually dimorphic traits
of the camellia weevil and the thickness of camellia peri-
carps in populations without weevils, we show some lines
of novel evidence that bizarre morphologies of the weevil
and the plant have evolved through a reciprocal adaptive
process. Second, the heritability of camellia pericarp thick-
ness is estimated using a method based on molecular ge-
netic markers (Ritland 2000) to further discuss the evo-
lution of the plant defense. Third, we examine the
relationship between local climatic conditions and the level
of camellias resource investment to defense. In this anal-
ysis, we compare camellia populations with and without
weevils, thereby inferring the defenseless phenotype that
probably represents the minimum thickness of pericarps
required for buffering external environmental stresses
other than infestation by the camellia weevil. Finally, in
conjunction with our previous phylogeographic studies on
the system (Toju and Sota 2006c, 2009), we discuss how
the weevil-camellia coevolutionary interaction has re-
sponded to global climate change during the last glacial
and postglacial periods. Our analysis concludes by pro-
posing that even slight changes in climate can dramatically
alter coevolutionary dynamics, thereby altering the various
ecological functions of biological interactions.
Material and Methods
Study System
The Japanese camellia is an evergreen broad-leaved tree
that is common in warm-temperate forests in Japan, Ko-
rea, and Taiwan. Seeds of this plant are attacked by a weevil
species, the camellia weevil, whose larvae grow by exclu-
sively infesting the plant seeds. This weevil is an agricul-
tural pest of Japanese camellia seeds (Saito and Suzuki
1982). Females of the weevil are characterized by their
very long snouts, which they use to bore through the thick
fruit coats (pericarps) of camellias to make holes that are
used for oviposition (g. 1A1G). After the maturation of
seeds, the woody, hard pericarps dehisce and seeds fall to
the ground (g. 1B). Larvae of a lepidopteran species and
unknown birds occasionally bore the camellia pericarp and
utilize the seed as a (presumably temporary) food source.
However, predation by those species is very rare (Toju
2008; H. Toju, personal observation) compared to that by
the camellia weevil.
Our previous studies (Toju and Sota 2006a, 2006b)
showed that the pericarp thickness of the Japanese camellia
was positively correlated with the snout length of female
camellia weevils across populations over a 700-km transect
in Japan, suggesting that the plant had been involved in
an evolutionary interaction with the camellia weevil. In
fact, an analysis of natural selection revealed that the weevil
exerted geographically variable selection pressure on ca-
mellia pericarps, potentially promoting the adaptive di-
versication of the plant populations (Toju and Sota
2006b; Toju 2007). Given that gene ow between popu-
Figure 1: Study system. A, Female (below) and male (above) camellia weevils. B, Japanese camellia fruit. After seed maturation, camellia
fruits dehisce (upper right), and seeds attached to the fruit columns fall to the ground. C, Cross section of a camellia fruit. D, Female weevil
boring into a camellia fruit. Arrows indicate bores made by the weevil. E, Female weevil inserting its ovipositor into a camellia fruit. F,
Snout length of a female weevil. G, Ovipositor length. Red lines indicate the length of the chitinous fragment supporting the distal half of
soft ovipositor tissue (ovipositor length in this study). A dissected ovipositor is also shown with a head (lower left). H, Study sites. The
morphological analysis of the Japanese camellia populations was conducted with (red) and without (blue) the camellia weevil. See table A2
in the online edition of the American Naturalist for the abbreviation of islands. Yellow circles indicate the study sites for the weevil
morphological analysis (table A1). I, Sexual dimorphism of weevil snout length. In each sex, snout length (SD) was regressed against the
pericarp thickness of sympatric camellias across populations (pink p female; cyan p male). The dashed line indicates an experimentally
estimated line on which half of weevil boreholes are expected to reach seeds (Toju and Sota 2006b). At the right side of this line, camellias
can defend against weevils attacks with a probability of more than 50% (Toju and Sota 2006b). J, Regression of weevil ovipositor length
(SD) against the pericarp thickness of sympatric camellias. K, Latitudinal gradient of armament escalation in weevils. Each female (pink)
and male (cyan) weevil snout length (SD) was regressed against latitude. L, Latitudinal gradient of weevil ovipositor length (SD). M,
Latitudinal gradient of armament escalation in camellias. Pericarp thickness was regressed against latitude (red p populations with
weevils; blue p populations without weevils). N, Geographic variation in the fruit center radius of camellias (red p populations with
weevils; blue p populations without weevils).
lations is restricted at very small spatial scales in both
species (e.g., !10 km; Ueno et al. 2000; Toju et al. 2011;
see also Toju and Sota 2006c, 2009), each population can
evolve in response to local coevolutionary selection. No-
tably, the level of the camellia defensive armament is higher
in lower-latitudinal and lower-altitudinal regions (Toju
and Sota 2006b; Toju 2008). This observation illuminates
the possibility that some kinds of climatic factors play
important roles in the geographic differentiation of the
weevil-camellia evolutionary interactions.
Geographic Variation in Weevil Snout and
Ovipositor Length
To explicitly examine the morphological adaptation of
weevils to sympatric camellia fruit morphology, we studied
geographic variation in the sexual dimorphism of snout
length (g. 1A, 1F) among populations throughout Japan
(g. 1H; table A1 in the online edition of the American
Naturalist). Morphological measurements were conducted
using the software ImageJ (National Institutes of Health)
on digital images taken with an S8APO/EC3 stereomicro-
scope (Leica Microsystems). After measuring snout length
(g. 1F), female abdomens were dissected to determine
ovipositor length. Although the ovipositor of the camellia
weevil is as long as the snout (g. 1G), the total length of
the ovipositor is difcult to measure because it is soft and
retractable. Therefore, the length of the chitinous fragment
supporting the distal half of the ovipositor (coxite; g. 1G;
Donaldson 1992) was measured. In each population, up
to 10 randomly chosen individuals for each sex were mea-
sured. The sex-dependent evolutionary effects of the Jap-
anese camellia on weevil snout length were tested by an
ANOVA model of snout length, including the factors of
sex, pericarp thickness of sympatric camellias (table A2 in
the online edition of the American Naturalist; see below),
and their interaction effects. Weevil snout length was also
regressed against camellia pericarp thickness across pop-
ulations in both sexes to test whether the evolutionary
response of weevil snout length to local camellia pericarp
thickness differed according to sex. Because female ca-
mellia weevils deposit eggs into camellia seeds, both snout
length and ovipositor length should evolve through in-
teractions with the Japanese camellia. The local adaptation
of ovipositors was tested by regressing ovipositor length
against camellia pericarp thickness across populations. The
statistical software R, version 2.9.1 (available at http://
www.r-project.org/), was used for statistical analyses.
Camellia Fruit Morphology
To determine whether the thickened camellia pericarp has
evolved as a defense against the camellia weevil, we next
compared fruit morphology among islands with or with-
out camellia weevils (g. 1H). From 2002 to 2007, fruits
of the Japanese camellia were collected from 49 popula-
tions throughout the Japanese archipelago shortly after the
oviposition season of the camellia weevil (table A2; g.
1H). The sampled area included islands on which the ca-
mellia weevil has not been reported (Fujimoto 2004). This
weevil is estimated to be absent from these islands because
it usually imposes severe predation pressure on camellia
seeds (Saito and Suzuki 1982; Toju and Sota 2006b), and
hence the weevil would have been reported as an agri-
cultural pest if it were present on the islands. To conrm
the presence or absence of the camellia weevil within each
camellia population, the number of boreholes was counted
on each fruit (g. 1D). The camellia weevil was considered
to be absent from populations with no boreholes on fruits
(table A2). The diameter and pericarp thickness of col-
lected fruits were measured as described elsewhere (Toju
and Sota 2006b). In addition, to compare the resources
allocated to pericarps (i.e., defense) with those allocated
to seeds (i.e., reproduction), the radius of fruit center (g.
566 The American Naturalist
1C; hereafter, fruit center radius) was calculated. To ex-
amine the evolutionary impact of the weevil on camellia
fruit morphology, geographic variation in pericarp thick-
ness or in fruit center radius was explained in an ANOVA
model, which included the effects of the presence/absence
of the weevil and sampling location (latitude and longi-
tude) and their interactions.
Heritable Variation in Camellia Pericarp Thickness
The heritability of pericarp thickness was estimated based
on genotyping using microsatellite markers (Ritland 2000).
For this analysis, we chose a camellia population in Ka-
wahara, Yakushima Island (YKI; g. 1H; table A2), which
exhibited the large phenotypic variation commonly ob-
served in populations on this island. Camellia fruits and
leaves were sampled from 76 trees within a 50-m radius,
and pericarp thickness was measured. Genomic DNA was
extracted from leaves and genotyping was performed using
29 microsatellite markers (table A3 in the online edition
of the American Naturalist). DNA extraction and geno-
typing procedures are detailed elsewhere (Ueno and Tsu-
mura 2009).
Based on the microsatellite genotypes, intertree pairwise
relatedness was inferred using the program Mark, version
3.1 (Ritland 2006). Heritability estimates were obtained
from a regression of intertree trait similarity against pair-
wise relatedness using the Mark program. The phenotypic
similarity of pericarp thickness P for two trees i and j was
represented by
(P U)(P U)
i j
Z p , (1)
ij
V
where U and V are the mean and variance of P in the
population, respectively. Assuming that phenotypic simi-
larity is determined by the sharing of both genes and en-
vironments, it is expressed as
2
Z p2r h r e , (2)
ij ij e ij
where r
ij
is the relatedness coefcient, h
2
is heritability,
r
e
is the correlation due to shared environment (assumed
constant for all tree pairs), and e
ij
is random error. Note
that the Mark program can incorporate the effects of
distance-related similarity/dissimilarity of environmental
conditions by adding the term b
e
d
ij
, where b
e
is the co-
efcient of linear decrease of environmental correlation
between two individuals separated by the distance d
ij
(Rit-
land 2006). However, our preliminary analysis showed that
the b
e
coefcient was nonsignicant; hence, the term b
e
d
ij
was not considered.
For each of the four relatedness estimators (Queller and
Goodnight 1989; Ritland 1996; Lynch and Ritland 1999;
Wang 2002), heritability was estimated as
Cov (r , Z )
ij ij
2
h p , (3)
2 Var (r )
ij
where is the covariance between relatedness Cov (r , Z )
ij ij
and phenotypic similarity, and is the actual vari- Var (r )
ij
ance of relatedness, whose calculation is detailed elsewhere
(Ritland 2000).
Climatic Gradient
Our previous study (Toju and Sota 2006b) showed that
features of the weevil-camellia evolutionary interaction
varied gradually along latitude across the Japanese islands.
Since climatic environments are expected to vary along
latitude, we rst analyzed the latitudinal gradient of of-
fensive (i.e., weevil snout and ovipositor length) and de-
fensive (camellia pericarp thickness) armament by regress-
ing each trait size on latitude across populations. In
addition, to elucidate how investment to seeds differs
among camellia populations, fruit center radius was re-
gressed against latitude as well.
To examine how resource allocation to the pericarp de-
pended on local climate, we focused on geographic vari-
ation in annual mean temperature, annual precipitation,
and annual mean solar radiation (meteorological data
from the Japan Meteorological Agency 2002). Across pop-
ulations, a regression of pericarp thickness on each climatic
variable was conducted. We predicted that pericarp thick-
ness would show gradients along the climatic variables
across camellia populations with weevils if resource allo-
cation to defense was affected by local climatic environ-
ments. In contrast, across populations without weevils, the
trait was expected to show little geographic variation. To
test this potential difference in resource allocation to de-
fense between populations with and without weevils, we
analyzed an ANOVA model that included the interaction
terms of climatic variables and the existence of weevils.
In addition to the climatic gradient of the camellia
defensive trait, we analyzed the gradient of the weevil-
camellia evolutionary/ecological interactions. First, we
predicted that balance between weevil and camellia ar-
mament, which could determine the nature of local eco-
logical interactions (Toju and Sota 2006b; Toju 2009),
would vary along the cline of climatic conditions. The
differential effects of climatic environment on weevil and
camellia armament size were examined in an ANOVA, in
which species identity (weevil or camellia) and three cli-
matic variables and their interaction terms were incor-
porated as explanatory variables. For weevils, published
data of female snout length in 21 populations (Toju and
Table 1: Analysis of geographic variation in camellia
fruit morphology
Variable df F P
Pericarp thickness:
Weevil
a
1 29.3 !.0001
Latitude
a
1 92.9 !.0001
Longitude 1 .1 .7540
Weevil # latitude
a
1 4.6 .0386
Weevil # longitude 1 .4 .5358
Fruit center radius:
Weevil
a
1 4.4 .0410
Latitude
a
1 4.6 .0377
Longitude
a
1 7.4 .0093
Weevil # latitude 1 .7 .3950
Weevil # longitude 1 .9 .3384
Note: In an ANOVA model, geographic variation in pericarp
thickness was explained by the presence/absence of the camellia
weevil (weevil effect), latitude, longitude, and the interaction
terms of the weevil effect and geographic locations (top). Con-
comitantly, geographic variation in fruit center radius, which rep-
resented the amount of resources allocated to seeds, was explained
by the explanatory variables in another ANOVA model (bottom).
The data of 49 camellia populations (32 populations with weevils
and 17 populations without weevils) were analyzed.
a
Coefcient included in a stepwise-selected model based on
Akaikes Information Criterion.
Sota 2006a, 2006b; Toju 2008) with additional snout length
data in 14 populations were subjected to the ANOVA(table
A4 in the online edition of the American Naturalist). For
camellias, the data of 32 populations with the camellia
weevil were used. Second, contribution of climatic envi-
ronment to local weevil-camellia ecological interactions
was inferred. Two response variables were prepared. The
one is the proportion of successful weevil boreholes (i.e.,
the proportion of the number of holes reaching seeds to
the total number of holes analyzed; g. 1D), and the other
is the proportion of mature seeds infested by camellia
weevil larvae (i.e., the ratio of the number of infested seeds
to the total number of seeds analyzed). For each fruit
collected in each population, the number of boreholes
made by weevils (g. 1D) and that of boreholes reaching
seeds were counted. Likewise, the number of intact/in-
fested mature seeds was counted as well. In total, 26,354
boreholes, of which 11,199 reached the seeds, and 8,820
mature seeds, of which 1,764 seeds were infested (28 pop-
ulations with weevils; table A2), were subjected to multiple
regression analyses, in which effects of three climatic var-
iables were examined (generalized linear models with bi-
nomial error and logit-link functions). Third, association
between each climatic variable and each evolutionary/eco-
logical variable was graphically presented on the basis of
a series of univariate regressions.
Results
Geographic Variation in Weevil Snout and
Ovipositor Length
When weevils were collected within an area in which the
camellia population featured very thick pericarps, the
snouts of female weevils were 3.1-fold longer than those
of males (g. 1I). In contrast, weevil sexual dimorphism
was only moderate when collected from areas dominated
by camellias with thin pericarps (g. 1I). Although both
female and male snout lengths were correlated with ca-
mellia pericarp thickness across 11 populations (female:
, , snout p0.623 #pericarp 5.81 F p139.3 P !
1, 9
; male: , , .0001 snout p0.049 #pericarp 5.39 F p7.4
1, 9
), the regression slopes were steeper in females P ! .0239
than in males ( , ). Moreover, ovi- F p105.6 P ! .0001
1, 18
positor length (g. 1G) increased signicantly with in-
creasing camellia pericarp thickness across populations
( , , ovipositor p0.146 #pericarp 4.85 F p73.8 P !
1, 9
; g. 1J). .0001
Camellia Fruit Morphology in Populations
with or without Weevils
A morphological analysis of camellias indicated that mean
pericarp thickness across populations with weevils was
10.34 mm ( mm), while that across populations SD p5.31
without weevils was 6.25 mm ( mm). An SD p1.13
ANOVA showed that camellia populations exposed to wee-
vils showed signicant increases in pericarp thickness com-
pared with populations from which weevils were absent
(table 1). The analysis also indicated signicant effects of
latitude and the interaction between latitude and the pres-
ence/absence of camellia weevils (table 1; see below for
detailed discussion). In contrast, mean fruit center radius
across camellia populations with weevils was 10.95 mm
( mm), smaller than that across populations SD p1.34
without weevils ( mm, mm). mean p11.62 SD p0.71
The effect of the presence/absence of weevils on fruit cen-
ter radius was signicant but weak (table 1).
Heritable Variation in Camellia Pericarp Thickness
A genetic analysis using 29 microsatellite markers among
a population of 76 camellia plants demonstrated that peri-
carp thickness was heritable (table 2). Heritability esti-
mates ranged from 0.63 to 0.82 ( ), depending mean p0.74
on relatedness estimators (table 2).
Table 2: Heritability estimates of camellia pericarp thickness based on genetic analysis
using 29 microsatellite markers
h
2
r
e
Relatedness estimator Estimate SE P Estimate SE P
Queller and Goodnight 1989 .80 .52 .0324 .014 .008 .0570
Ritland 1996 .82 .61 .0432 .013 .057 .0242
Lynch and Ritland 1999 .70 .55 .0449 .009 .008 .0530
Wang 2002 .63 .45 .0501 .011 .006 .0016
Note:: Heritability (h
2
) and the coefcient of shared environment (r
e
) were estimated based on each
of four relatedness estimators. The reliability of the estimates was evaluated by the bootstrap sampling
of tree pairs (10,000 replicates).
Table 3: Effects of climatic environment on weevil/camellia ar-
mament size
Variable df F P
Camellia populations with weevils vs.
populations without weevils:
Weevil
a
1 25.5 !.0001
Temperature
a
1 54.7 !.0001
Precipitation
a
1 13.9 .0006
Solar radiation 1 .4 .5368
Weevil # temperature 1 4.9 .0331
Weevil # precipitation
a
1 7.3 .0100
Weevil # solar radiation 1 .4 .5137
Weevil populations vs. camellia popu-
lations with weevils:
Species
a
1 5.1 .0277
Temperature
a
1 60.8 !.0001
Precipitation
a
1 34.6 !.0001
Solar radiation 1 .3 .5704
Species # temperature
a
1 6.2 .0155
Species # precipitation 1 .2 .6767
Species # solar radiation 1 .1 .7881
Note: In an ANOVA model, geographic variation in pericarp thickness
was explained by the presence/absence of the camellia weevil (weevil effect),
three climate variables, and the interaction effects of the weevil effect and
respective climatic variables (top). The data of 49 camellia populations (32
populations with weevils and 17 populations without weevils) were analyzed.
In addition, differential effects of climatic environment on weevil/camellia
armament size were examined in another ANOVA model, in which species
identity (species effect), three climatic variables, and the interaction effects
of the species effect and respective climatic variables were incorporated as
explanatory variables (bottom). The data of 32 camellia and 35 weevil pop-
ulations were subjected to the analysis.
a
Coefcient included in a stepwise-selected model based on Akaikes In-
formation Criterion.
Climatic Gradient of the Arms Race
Regression analyses revealed that the snout length of
female weevils increased at lower latitudes (snout p
, , ), whereas 1.23 #latitude 52.9 F p17.5 P p.0024
1, 9
male snout length did not ( - snout p0.086 #lati
, , ; g. 1K). Ovipositor tude 8.76 F p3.0 P p.12
1, 9
length also exhibited a latitudinal gradient (oviposi-
, , ; tor p0.290 #latitude 16.0 F p16.0 P p.0031
1, 9
g. 1L). Likewise, in camellias, pericarp thickness increased
at lower latitudes (populations with weevils; pericarp p
, , ; popula- 1.87 #latitude 72.2 F p67.2 P ! .0001
1, 30
tions without weevils, pericarp p0.70 #latitude
, , ; g. 1M). Notably, at higher 29.5 F p13.8 P p.0021
1, 15
latitudes, pericarp thickness was comparable between
populations with and without the camellia weevil,
whereas it diverged considerably at lower latitudes (sig-
nicant weevil # latitude effect in table 1; g. 1M). In
contrast, only marginally signicant association between
fruit radius center and latitude was observed (populations
with weevils; fruit center radius p0.22 #latitude
, , ; populations without weevils, 18.3 F p5.3 P p.0279
1, 30
, , fruit center radius p0.33 #latitude 0.62 F p5.7
1, 30
[these regressions are nonsignicant at P p.0311 a p
after Bonferroni correction]; g. 1N; table 1). 0.05
Across populations with weevils, pericarp thickness sig-
nicantly increased with increasing annual mean temper-
ature, while across populations without weevils, this pat-
tern was nonsignicant (g. 2A). Pericarp thickness also
increased with increasing annual precipitation across pop-
ulations with weevils, although it decreased with increasing
precipitation across populations without weevils (g. 2B).
An ANOVA revealed that the gradients along precipitation
were signicantly different between populations with and
without weevils (table 3). In contrast to the two climatic
variables, annual mean solar radiation did not signicantly
explain geographic variation in pericarp thickness among
camellia populations with weevils (g. 2C; table 3).
The snout length of female camellia weevils signicantly
increased with increasing annual mean temperature, but
the slope of the gradient was signicantly shallower than
that of camellia populations with weevils (g. 2D; see spe-
cies # temperature interaction in table 3). Thus, balance
between weevil and camellia armament varied along the
climatic gradient. Although female snout length signi-
cantly increased with increasing annual precipitation too,
the trait was not correlated with annual mean solar ra-
diation (g. 2E, 2F; table 3).
Our analysis also showed that the ecological interaction
Figure 2: Dependence of the weevil-camellia coevolutionary process on climatic conditions. AC, Relationship between camellia pericarp
thickness and each climatic variable (A, annual mean temperature; B, annual precipitation; C, annual mean solar radiation). The red lines
represent signicant regression ( ) across camellia populations with weevils, and the blue lines indicate regression across populations P ! .01
without weevils (see table 3 for the result of a multivariate model). DF, Relationship between the snout length of female weevils and each
climatic variable. In each panel, the regression of weevil snouts (triangles) is shown with that of camellia pericarps (circles; populations with
weevils). GI, Relationship between the percentage of the successful excavations of camellia pericarps by weevils and each climatic variable.
See table 4 for the result of a multivariate model. JL, Relationship between the proportion of seeds infested by weevil larvae and each
climatic variable.
Table 4: Effects of local climatic conditions on the weevil-camellia interaction
Proportion of successful
excavations
a
Proportion of infested seeds
b
Variable Coefcient z P Coefcient z P
Temperature .485 (.023) 21.5 !.0001
c
.368 (.047) 7.8 !.0001
c
Precipitation .270 (.019) 14.3 !.0001
c
.027 (.041) .7 .513
Solar radiation .177 (.018) 9.6 !.0001
c
.056 (.035) 1.6 .106
c
Note: The proportion of successful excavations or the proportion of infested seeds was regressed on three
climatic variables (multivariate regressions). All climatic variables were z-standardized before regression. In each
regression, a generalized linear model with binomial error and a logit-link function was constructed.
a
In total, the data of 26,354 boreholes, of which 11,199 reached the seeds, were collected from 28 populations
and subjected to the analysis.
b
In total, the data of 8,820 seeds, of which 1,764 were infested, were collected from 28 populations and
subjected to the analysis.
c
Coefcients included in stepwise-selected models based on Akaikes Information Criterion.
between weevils and camellias varied along the gradient
of climatic conditions. The percentage of the successful
excavation of the camellia pericarp by weevils decreased
from 90% to 20% as annual mean temperature, annual
precipitation, and annual mean solar radiation increased
(g. 2G2I; see g. A1 in the online edition of the American
Naturalist for a regression by latitude). A multivariate re-
gression revealed that effects of all three climatic variables
were signicant and that annual mean temperature had
the largest effect among the variables (table 4). The in-
festation ratio of camellia seeds by weevil larvae also de-
creased with increasing annual mean temperature, annual
precipitation, and annual mean solar radiation (g. 2J2L;
g. A1). However, only the effect of annual mean tem-
perature was signicant in a multivariate regression model
(table 4).
Discussion
Our results showed that the level of resource allocation to
the heritable defensive traits of preys/hosts was related to
local climate and that such environmental dependence of
prey/host evolutionary processes could promote the geo-
graphic differentiation of coevolutionary arms races with
their predators/parasites. Moreover, analyses of climatic
gradients also showed that the climatic dependence of co-
evolutionary processes could organize geographic varia-
tion in the success of predator/parasite attacks or preda-
tion/parasitization intensity, further structuring the
geographic mosaics (or clines) of evolutionary and eco-
logical interactions between species. These ndings shed
light on the potential effects of climatic change on coevo-
lutionary interactions in nature, providing the viewpoint
of spatiotemporally dynamic processes of interspecic in-
teractions. In the following discussion, we examine how
coevolving traits and evolutionary/ecological processes
vary along climatic gradients and consider how coevolu-
tionary processes respond to climate change, by inferring
the history of the weevil-camellia interaction during past
glacial/postglacial periods.
Climatic Gradients of Arms Race Coevolution
We found that the extent of the weevil-camellia arms race
differed signicantly along a latitudinal gradient of climatic
environments (g. 1K1M). Given that climatic conditions
can strongly affect the photosynthetic activity of the Jap-
anese camellia (e.g., higher photosynthetic rate at higher
temperature; Miyazawa and Kikuzawa 2006; Y. Miyazawa
and H. Toju, unpublished data), the resource availability
of the plant is a potential key factor of the geographically
structured coevolutionary interactions. There are some hy-
potheses explaining this productivity gradient. For ex-
ample, when a prey species is resource limited, the trade-
off between defensive trait size and the maintenance/
production of vegetative and reproductive parts can limit
investment to defense; in contrast, if the prey species can
gain access to sufcient resources, evolutionary escalation
of prey defense and the counterevolution of predator of-
fense can occur (Sasaki and Godfray 1999). Therefore, the
climate-dependent investment to the pericarp (g. 2A, 2B)
likely represents an environment-dependent defense strat-
egy by camellias, which regulates the extent of coevolu-
tionary armament escalation. Interestingly, in populations
under relatively cool and arid climate, camellias invest-
ment in pericarps was low irrespective of the presence/
absence of the camellia weevil (g. 2A, 2B). This result
suggests that these camellia populations show the de-
fenseless phenotype that probably represents the mini-
mum thickness of pericarps required for buffering physical
environmental stresses such as frost damage. In contrast,
in populations under a warm, humid climate, investment
in pericarps diverged considerably among populations
with weevils (g. 2A). In the populations, camellias have
likely been selected to invest resources in defense, thereby
triggering the coevolutionary arms race with weevils. Con-
sequently, the remarkable diversity of the weevil-camellia
evolutionary interactions within a narrow range of inter-
mediate temperatures (g. 2A, 2D) may be attributed to
the existence of the threshold climatic condition that bi-
furcates the defenseless and escalation strategies by
camellias.
Alternatively, favorable climatic conditions may allow
the high population growth rate of the plant, which in
turn causes the rapid growth of weevil populations and
results in transiently severe seed infestation by weevils (cf.
Brockhurst et al. 2003). Such climate-dependent strength
of seed predation would determine the strength of natural
selection on the camellia defensive trait, thereby generating
geographic variation in the extent of the weevil-camellia
arms race (see Hochberg and van Baalen 1998 for theo-
retical discussion). Note that the severity of seed infesta-
tion decreased in the populations exhibiting higher tem-
peratures (g. 2J; table 4) and that this result seemingly
does not support this second hypothesis. Extensive the-
oretical studies that incorporate essential characteristics of
the weevil-camellia system will help to further test the
alternative hypotheses.
Ecological Consequences of Escalatory Coevolution
Our results further suggest that the climate dependence
of coevolutionary dynamics controls the ecological pro-
cesses of interacting species, as evidenced by the fact that
the average success of weevil boring decreased sharply with
increased temperature, precipitation, and quantity of solar
radiation (g. 2G2H). Although snout and ovipositor
length in female weevils have counterevolved in response
to camellia pericarp thickness (g. 1I, 1J), the balance
between predator weapon and prey armament changes as
the arms race proceeds (Toju and Sota 2006b; g. 2D).
Because long weevil snouts can incur mortality costs
(Menu 1993) and ovipositor length is constrained by total
body size, which is in turn limited by larval food sources
(i.e., camellia seed size), having longer snouts would be-
come increasingly costly. The resultant shift in the balance
between weevil weapon and camellia armament (g. 2D;
cf. Hanin et al. 2008) would decrease the mean success
rate of weevil attacks (g. 2G). As we observed, the severity
of seed infestation by weevil larvae decreased along the
climatic gradient (g. 2J), suggesting that a decrease in the
reproductive success of individual females (g. 2G) may
have resulted in lower population densities of the camellia
weevil.
Theory predicts that such escalatory coevolution likely
entails the alternation of interspecic ecological interac-
tions, which in turn can inuence natural selection pro-
cesses (Thompson 1999; Nuismer and Thompson 2006).
In particular, the emergence of highly defended hosts
through coevolution can promote the shifts of parasites
to less defended host species, thereby establishing new eco-
logical and evolutionary interactions. This theory of co-
evolutionary alternation (Thompson 1999; Nuismer and
Thompson 2006) deserves extensive future studies that
simultaneously investigate the geographically divergent
processes of escalatory coevolution and the host-shift dy-
namics of interacting species.
Climatic Change and Coevolutionary Processes
The observed climatic dependence of the arms race process
leads to the proposition that climate change has played
essential roles in the (co-)evolutionary history of weevil
and camellia species. For example, change in air temper-
ature during the last glacial-interglacial cycle could have
greatly contributed to the geographic structuring of the
weevil-camellia coevolutionary interactions. Paleoclimatic
and phylogeographic studies suggested that the Japanese
camellia and the camellia weevil were restricted to a few
narrow refugia in the southern part of Japan during the
last glacial period and that the two species were under a
cool climate during the period (Hoshiai and Kobayashi
1957; Tsukada 1983, 1985; Toju and Sota 2006c; g. 1H).
A population genetic analysis of the camellia weevil further
inferred that the camellia weevil was restricted to a narrow
range in southern Kyushu during the glacial period and
that populations of the species rapidly diverged after the
last glacial maximum (approximately 18,000 years ago;
Toju and Sota 2009; g. 1H). Given the environmental
dependence of the weevil-camellia evolutionary interac-
tion (g. 2), it is presumable that weevils and camellias
had not evolved exaggerated armaments during the last
glacial period. As global climate changed after the glacial
age, the camellias that remained in the south likely ex-
perienced an increase in air temperature and initiated the
arms race coevolution with weevils. In contrast, the ca-
mellia populations expanding their range toward the north
have not experienced an increase in temperature and may
have retained the ancestral state of the evolutionary/eco-
logical interactions with weevils. This putative spatiotem-
poral process of the weevil-camellia interaction implies
that dynamics of interspecic interactions can change con-
siderably in the wild, depending on the spatial variation
or temporal change of climatic environments.
Overall, this study demonstrates that coevolutionary dy-
namics and subsequent ecological interactions between
species can shift markedly within relatively narrowclimatic
ranges (g. 2). Such climatic gradients of the evolutionary
and ecological processes of interacting species are poten-
tially important in broad types of natural communities
(Bertness et al. 1981; Sanford et al. 2003; Pennings et al.
2009; see also Andrew and Hoghes 2005), though the im-
portance of (co-)evolutionary dynamics in this context has
not been thoroughly tested in most interspecic interac-
tions. Considering that by the end of this century air tem-
perature is expected to increase by 1.1 to 6.4C compared
with the range observed between 1980 and 1999 (Solomon
et al. 2007), global warming may greatly alter the evolu-
tionary and ecological processes of interspecic interac-
tions. Consequently, to understand the impacts of climate
change on natural communities, not only the ecological
processes of single species but the coevolutionary dynamics
of interacting species must be considered.
Acknowledgments
We thank Y. Komatsu and Y. Tsumura for supporting mo-
lecular experiments and L. Kawaguchi for providing a pho-
tograph of a camellia fruit. We are also grateful to the
anonymous reviewers for their helpful comments on the
manuscript. This study is partly supported by the Japan
Society for the Promotion of Science (Fellowship for Young
Researchers: 1702263).
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