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Ecology Letters, (2010) 13: 383393

doi: 10.1111/j.1461-0248.2009.01433.x

REVIEW AND
SYNTHESIS

Sofia Gripenberg,1* Peter J.


Mayhew,2 Mark Parnell2 and
Tomas Roslin3
1

Department of Zoology,
University of Oxford, South
Parks Road, Oxford OX1 3PS, UK
2

Department of Biology,

University of York, PO Box 373,


York YO10 5YW, UK
3

Metapopulation Research

Group, Department of
Biological and Environmental
Sciences, PO Box 65 (Viikinkaari
1), 00014 University of Helsinki,
Finland
*Correspondence: E-mail:
sofia.gripenberg@zoo.ox.ac.uk

A meta-analysis of preferenceperformance
relationships in phytophagous insects
Abstract
The extent to which behavioural choices reflect fine-tuned evolutionary adaptation
remains an open debate. For herbivorous insects, the preferenceperformance
hypothesis (PPH) states that female insects will evolve to oviposit on hosts on which
their offspring fare best. In this study, we use meta-analysis to assess the balance of
evidence for and against the PPH, and to evaluate the role of individual factors proposed
to influence host selection by female insects. We do so in an explicitly bitrophic context
(herbivores versus plants). Overall, our analyses offer clear support for the PPH:
Offspring survive better on preferred plant types, and females lay more eggs on plant
types conducive to offspring performance. We also found evidence for an effect of diet
breadth on host choice: female preference for good quality plants was stronger in
oligophagous insects than in polyphagous insects. Nonetheless, despite the large
numbers of preferenceperformance studies conducted to date, sample sizes in our
meta-analysis are low due to the inconsistent format used by authors to present their
results. To improve the situation, we invite authors to contribute to the data base
emerging from this work, with the aim of reaching a strengthened synthesis of the
subject field.

Present address: Tomas Roslin,

Department of Applied Biology,


PO Box 27 (Latokartanonkaari
5), FI-00014 University of
Helsinki, Finland

Keywords
Mother knows best principle, female preference, herbivore, host selection, metaanalysis, nave adaptationist hypothesis, offspring performance, optimal oviposition
theory, plant quality.
Ecology Letters (2010) 13: 383393

INTRODUCTION

Although behavioural and evolutionary ecologists have long


been studying the principles dictating resource use by
heterotrophs, the extent to which behavioural choices
reflect fine-tuned evolutionary adaptation remains an open
debate (e.g. Jaenike 1978; Pyke 1984; Charnov & Stephens
1988; Mangel 1989; West & Sheldon 2002; Shuker & West
2004; Burton-Chellew et al. 2008). In the context of plant
insect interactions, host selection by ovipositing females
offers a central theme (Bernays & Chapman 1994; Schoonhoven et al. 2005; Tilmon 2008). Here, the range of
patterns detected has stimulated a wide range of theories on
forces moulding female choice with respect to offspring
performance (reviewed by e.g. Thompson 1988; Courtney &
Kibota 1990; Jaenike 1990; Mayhew 1997; Craig & Itami
2008).

The basic premise: female preference reflects offspring


performance

From an evolutionary perspective, the basic setting for host


plant choice is a simple one: given that plants differ in their
suitability as food for insects, and that the immature stages
of developing insects are often rather immobile, natural
selection should favour females with an ability to discriminate between hosts of different suitability for larval
development (Levins & MacArthur 1969; Jaenike 1978;
Thompson 1988; Mayhew 1997). According to the preferenceperformance hypothesis (also known as the nave
adaptionist hypothesis or the mother-knows-best hypothesis), females will then maximize their fitness by laying their
eggs on plant types on which their offspring perform
the best. This is our first, general hypothesis (H1; Table 1)
that female preference reflects offspring performance, as dictated by
 2010 Blackwell Publishing Ltd/CNRS

384 S. Gripenberg et al.

Review and Synthesis

Table 1 Hypotheses tested in this study along with specific predictions

Hypothesis

Prediction

H1. Female preference reflects offspring performance


H2. Preferenceperformance coupling is modified
by ecological and or life history factors

P1.1
P2.1
P2.2
P2.3
P2.4
P2.5
P2.6

the quality of the host plant. From this, we also derive our first
testable prediction: that setting any effects of natural
enemies and competitors on performance aside offspring
will perform better on plants chosen by females (prediction
P1.1, Table 1).
Numerous studies have empirically assessed the relationship between female preference and offspring performance.
In some cases, female choice seems clearly adaptive, with
offspring performance being high on plant types preferred
by the females. Nevertheless, tens of studies report cases
where female preference and performance appear uncoupled, or where the relationship is surprisingly weak (e.g.
Rausher 1979; Valladares & Lawton 1991; Underwood
1994; Fritz et al. 2000; Faria & Fernandes 2001). What
factors may explain such apparent contradictions?
The plot thickens: the strength of the preference
performance relationship is modified by ecological and or
life-history factors

Several evolutionary and ecological considerations have


been proposed to explain apparent mismatches between
choice and performance (Thompson 1988; Courtney &
Kibota 1990; Thompson & Pellmyr 1991; Mayhew 1997;
Craig & Itami 2008). Our second general hypothesis (H2;
Table 1) is then that the strength of the general preference
performance relationship is modified by ecological and or life-history
factors. To specify this general notion into testable predictions, we will next pool factors proposed to cause deviations
from the preferenceperformance association into two
groups, depending on whether (1) there is a true lack of
preferenceperformance link and female choice is not
adaptive, or (2) there is no link between female preference
and host plant quality from the offsprings perspective, but
female choice is still adaptive in other ways. We will then
identify factors likely to accentuate a positive coupling
between preference and performance. For each of these
considerations, we derive a specific prediction (P2.1P2.6;
cf. Table 1) which we test by meta-analysis. In this context,
we note that the literature offers many further predictions
(see the above-mentioned review papers) but for the sake
 2010 Blackwell Publishing Ltd/CNRS

Offspring performance higher on preferred plants


Coupling tighter with narrower diet
Coupling tighter on woody than on herbaceous plants
Coupling tighter for sessile than for mobile offspring
Coupling tighter for gregarious than for solitary offspring
Coupling tighter for non-feeding than for feeding adults
Coupling tighter across than within plant species

of conciseness, we have restricted our survey to ideas for


which we have been able to obtain quantitative data for
preliminary assessment.
Female choice is non-adaptive and there is a true lack of
preferenceperformance coupling
As evolutionary change will always start with the raw
material provided by past evolution, and as organisms
evolve as wholes rather than as independent parts, several
factors may constrain evolution from reaching an optimal
solution (Gould & Lewontin 1979). In the context of female
choice, several constraints may emerge from limitations on
the information processing capacity of the insect nervous
system (e.g. Levins & MacArthur 1969; Fox & Lalonde
1993; Bernays 1998; Janz 2003; Egan & Funk 2006). If
selecting between plants becomes more complex the more
characteristics they differ in, then one may predict that the
link between female preference and offspring performance
varies with the degree of diet specialization (prediction P2.1,
Table 1). Monophagous insects would then be predicted to
be better decision-makers than insects with a broader diet,
because appropriate decisions would seem harder to make
for females faced with multiple stimuli. A similar relationship between diet breadth and choosiness might arise from
several additional physiological mechanisms and morphological characters, allowing taxa with fewer hosts to be more
finely tuned to them, as opposed to generalized adaptations
or plasticity expected in polyphages (e.g Roslin & Salminen
2008 with references therein).
Even in cases where insects are not trapped by
evolutionary or physiological constraints, preference and
performance may not necessarily be linked. For example, as
it may take many generations for evolution to filter out
females that choose poor quality hosts, the preference
performance link can be weak (or even negative) where
insects interact with novel plant species (Chew 1977;
Thompson 1988). As another example, if the relative quality
of host plant types varies unpredictably in time, females may
fail to evolve an ability to choose the plant type that would
be most suitable for their developing offspring (Cronin et al.
2001; Gripenberg et al. 2007a). If female choice is con-

Review and Synthesis

strained by temporal variation in host plant quality, we may


predict that females may find it particularly difficult to assess
the quality of herbaceous plants (Craig & Itami 2008),
because they are thought to change more during a growing
season than are woody plants (but see Salminen et al. 2004;
Gripenberg et al. 2007b). We test this prediction as P2.2
(Table 1).
Female behaviour may be adaptive although it is not manifested in
selecting for food quality
Most studies assessing the relationship between female
preference and offspring performance do so by asking
whether females rank their host plants based on their food
quality for offspring. Nevertheless, neither female choice
nor offspring performance takes place in isolation, but in
ecological contexts rendered more complex by an unequal
distribution of host plants, microclimatic conditions, mutualists, competitors and or natural enemies. While many
studies explicitly assume that females base their choice on
the quality of the plants, the distribution of other taxa may
also have a profound impact on both female preference and
offspring performance (e.g. Lima & Dill 1990; Nomikou
et al. 2003; Heisswolf et al. 2005; Van Mele et al. 2009).
Thus, a plant may be only marginally suitable as food, but
provide a safe haven from natural enemies (Bjorkman et al.
1997) or competitors (Wise & Weinberg 2002), or a source
of valuable mutualists (Atsatt 1981) and thus be highly
preferred for adaptive reasons. In this context, we note that
this study is explicitly focused on bitrophic interactions: on
whether variation in plant quality from an offsprings
perspective is reflected in female choice. While this solution
is dictated by practical considerations i.e. by the amount of
empirical studies accumulated to date the extent to which
natural enemies and competitors will mould preference
performance relations is an interesting question. From a
perspective of quantitative analysis, it will still have to wait
until further evidence has been accumulated.
Mechanisms promoting the formation of a positive preference
performance relationship
While the factors discussed above are likely to blur the link
between female preference and offspring performance,
other ecological traits may favour female choosiness. In
particular, limited offspring mobility has been highlighted as
a potentially important factor promoting female preference
for good quality hosts (Thompson 1988; Craig & Itami
2008). The extreme case is insects with sessile larvae (like
gallers and leaf miners), where larvae are confined to the
very resource unit selected by their mother, and where the
preferenceperformance coupling is thus expected to be
particularly strong. This generates prediction P2.3 (Table 1):
If limits to offspring mobility accentuate the importance of
female choice, we expect the strength of preference

Preferenceperformance in insects 385

performance coupling to be strongest in taxa with sessile


larvae.
Another factor hypothesized to favour a strong link
between preference and performance is the aggregation of
offspring. Selecting high-quality hosts may be more important for females laying their eggs in clutches than for females
distributing their eggs singly. In the former case, much
might be lost with a single bad decision, whereas the laying
of single eggs will be more akin to a risk-spreading strategy
(Mangel 1987; Hopper 1999). In that case, a few bad
decisions will result in the loss of few offspring only. This
equals prediction P2.4 (Table 1): If the aggregation of
offspring increases the variance in offspring performance,
the association between female preference and offspring
performance should be more accentuated in taxa laying their
eggs in batches than in taxa laying their eggs singly.
Finally, if insect females have the potential to feed as
adults, their fecundity may be less dependent on food
resources acquired at previous stages (e.g. Wheeler 1996;
Jervis et al. 2008). The potential for such refuelling is
expected to lessen the importance of larval food resources
on adult reproduction and longevity, and hence to weaken
the coupling between female preference and offspring
performance (P2.5, Table 1). A weaker association between
female preference and offspring performance in species
where adult females consume no food could also support
the notion of a conflict between parent and offspring: if
adults and offspring feed on different resources, females
may actually increase their fitness by being selfish at the
expense of the performance of their offspring (e.g. Jaenike
1986; Mayhew 2001; Scheirs & De Bruyn 2002; Janz et al.
2005).
Certain traits of the host plants may also promote a link
between female preference and offspring performance.
Naturally, the larger the difference in offspring performance
on different host types, the more likely are females to evolve
an ability to select hosts of high quality (Craig & Itami
2008). As one may intuitively assume that differences in
offspring performance are larger between than within plant
species, one might expect stronger evidence for the
preferenceperformance hypothesis to emerge from studies
assessing preferenceperformance relationships in an interspecific than an intraspecific setting (P2.6, Table 1).
Aims

Although preferenceperformance relationships have been


assessed in a large number of plantherbivore interactions,
empirical data to support or reject general hypotheses are
scattered. In this paper, we aim to assess (1) to what extent
the literature provides support for the overall preference
performance hypothesis as played out in a bitrophic setting
(H1; Table 1) and (2) the importance of selected biological
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386 S. Gripenberg et al.

factors proposed to influence the observed strength of


preferenceperformance relationships (H2; Table 1). Given
the rich body of theory and the vast literature on the topic,
the broader, systematic approach to testing general hypotheses about the evolution of preferenceperformance
relationships recently advocated by Craig & Itami (2008)
is admittedly challenging. Consequently, our intention is not
to provide an all-encompassing synthesis, but to complement previous narrative reviews on the subject. We focus on
the two general and six specific predictions derived from the
ideas discussed above (cf. Table 1), and use meta-analysis to
establish extant, quantitative support for each of them. For
practical reasons, our selection of hypotheses is rather based
on the availability of data to test them than on the current
status of each hypothesis.
METHODS

The relationship between female preference and offspring


performance can be seen from two perspectives: one can
either assess offspring performance in relation to the
choices made by females, or female responses in relation
to plants differing in their suitability as hosts for the
offspring. The general assumption in the PPH literature is
that differences in offspring performance generates a
selection pressure resulting in female preference, but still,
many studies conducted to date have used an inverse
approach: the authors have first established which plant is
preferred versus not preferred by the female, then compared
offspring performance between these plant types. Importantly, this is not the same as first establishing which plant
type the offspring performs best on, then testing whether
the female has generated a preference for it and in fact, the
two approaches could yield different conclusions. We
therefore performed two types of analyses, using either a
measure of offspring performance or of female preference
as the response. In the performance analyses, our aim was
to assess whether offspring perform better on host types
preferred by ovipositing females than on less preferred host
types. In the preference analysis, we tested whether females
are more prone to lay their eggs on host types on which
their offspring perform well than on host types of poorer
quality. As most studies assess the preferenceperformance
relationship on two or at most a few plant types, our
effect sizes are based on pairwise comparisons.
Data generation

To survey the literature on preference and performance, we


started out from studies collected for a previous narrative
review on the subject (Mayhew 1997), along with papers
collected for a preliminary meta-analysis on the topic
(Parnell 2004). These papers were obtained by searching
 2010 Blackwell Publishing Ltd/CNRS

Review and Synthesis

Entomology Abstracts in Cambridge Scientific Abstracts,


Blackwell Synergy, and Science Direct, using the search
terms oviposition preference, oviposition, host plant
preference, host selection and preferenceperformance.
Based on abstract and title information, 350 papers were
reviewed in depth to assess suitability. To include more
recent studies, we examined all papers having cited Mayhew
(1997) in ISI Web of Science (last accessed 2 September,
2009; n = 140 studies).
For a study to be included in our general data set, it
had to contain sufficient information to allow calculation
of the relevant effect size (see Performance analyses and
Preference analysis), and to allow the ranking of plants in
terms of preference and or performance (see Appendix S1). To avoid problems associated with pseudoreplication, we took a conservative approach and included
only one data point per insect species and published
study. In other words in cases where preference and
performance were assessed on more than two plant types,
we randomly chose one plant pair to be included in our
analyses. Information was extracted from both numerical
and graphical representations. When the information was
graphical (e.g. variation around a mean shown as error
bars), the image was digitized and data extracted using the
software ImageJ.
Specific criteria for inclusion of studies in individual
analyses are given below (Meta-analysis). In addition, we
excluded five types of studies which matched our general
criteria, but which we found too deviant to describe any
general associations between herbivorous insects and their
natural host plants. First, studies involving insects feeding
on dead plant material (such as logs and stored peas) were
excluded. Second, we excluded a number of studies in which
female preference for certain plant types had been inferred
from adult feeding preferences rather than from information on oviposition behaviour. Third, we excluded cases
where the host plant species upon which preference and
performance were tested was derived from an area well
beyond the current distributional range of the herbivore
(for such cases, observed preference will hardly reflect
recent selection pressures, because the insect will never
encounter the plant in nature). Fourth, to avoid the results
being influenced by the inclusion of negative controls (i.e.
plant species upon which the herbivore does not typically
feed), we excluded studies that include plant types that are
available, but not used as hosts in the field. Finally, studies
examining preference and performance on anthropogenic
cultivars were excluded, because the average length of such
plantherbivore associations is likely of younger origin than
the average length of extant insectplant associations.
As many studies reported multiple, partly overlapping
measures of preference and or performance, we used a
series of clear-cut criteria to reduce the number of non-

Review and Synthesis

independent data points. These criteria are identified in


Appendix S2.
Meta-analysis

Performance analyses
To compare performance on preferred versus non-preferred
plants, plant types were ranked according to how acceptable
they were among ovipositing females (Appendix S1).
Performance analyses were focused on three metrics derived
from the literature: Offspring survival, i.e. the fraction of
offspring surviving from the onset of a study until the
completion of the study (the exact period over which
survival was assessed varied among studies); size, often
assumed to reflect fitness (Honek 1993; Tammaru et al.
1996), and development time, reflecting the time the insect is
exposed to natural enemies and, for species with multiple
generations, the potential for population growth (e.g. Feeny
1976; Clancy & Price 1987; but see Benrey & Denno 1997;
Williams 1999).
For each performance metric, we derived a separate
metric of effect size. For survival data, we used the
(ln-transformed) odds ratio (Rosenberg et al. 2000). Thus,
for a study to be included in this analysis, it had to provide
sufficient information for us to infer the number of living
and dead individuals on the preferred and non-preferred
plant type. For offspring size, we used the standardized
difference (Hedges d; Hedges & Olkin 1985) between the
mean weights of offspring on plants preferred by females
and offspring on less preferred plant types. To be included
in this analysis, a study had to report the mean, a measure of
variation around this mean (SD or SE) and sample sizes for
offspring weight on two plant types differing in their
attractiveness to ovipositing females. For development time,
we used Hedges d of mean development time between
preferred and less preferred plant types as our effect size.
In each of the above analyses, we used the less preferred
plant type as the control group, and the more preferred
plant as the experimental group (Rosenberg et al. 2000).
Thus, for survival and weight, a positive effect size implies
that offspring fare better on the host type preferred by
females. As fast development is assumed to reflect higher
fitness, a negative effect will support the preference
performance hypothesis in the analysis of development
times.
Preference analysis
To assess whether female insects prefer host types on which
their offspring perform best, we compared the number (or
density) of eggs per plant unit between good quality and
bad quality plants (for a definition of good and bad
quality plants, see Appendix S1). Again, we used Hedges d
as our effect size (cf above), and defined the bad quality

Preferenceperformance in insects 387

plants as the control group, and the good quality plants as


our experimental group. Hence, here a positive effect size
will support the preferenceperformance hypothesis.
Statistical models
To examine the support for individual predictions (Table 1;
P2.1P2.6), we tested whether effect sizes differ among
studies assigned to different groups (Rosenberg et al. 2000).
To test P2.1, we classified target taxa as being monophagous, oligophagous or polyphagous. In this context, insects
specialized on a certain plant genus were classified as
monophagous, insect species feeding on plants from several
genera within a family as oligophagous, and insect species
known to feed on plant species from several families as
polyphagous. To test P2.2, we noted whether the studied
plants were woody or herbaceous. We tested P2.3 by
assigning the studied insect species to either of two broad
groups: free-feeding or sessile (the latter group consising of
leaf miners, gallers, stem borers and sap-suckers with
immobile immatures). To test P2.4, we noted whether
females lay their eggs in batches or as single eggs. To test
P2.5, we grouped studies according to whether the females
take up nutrients as adults. In cases where this information
was not explicitly mentioned, we assumed that species with
fully developed mouth parts do indeed feed as adults.
Finally, to test P2.6, we classified studies according to
whether the host plants compared were of the same or of
different species (i.e. whether the comparison was intra- or
interspecific). In cases where the information needed for
assigning studies to different groups was not available in the
primary publication, we contacted the authors for additional
information, or consulted with experts of the respective
taxonomic group.
As we were more interested in variation among effect
sizes than in group-specific means, we used random effects
models. For each response variable, we first conducted a
summary analysis with no data structure (i.e. no categorical
variables). If the total heterogeneity of the sample of effect
sizes (QT) was significant (indicating that there is structure
in the data not captured by such a simple model), we
conducted analyses with our set of pre-defined explanatory
variables (separate analyses for each explanatory factor). If
the between-group heterogeneity (QB) was significant, we
inferred that the mean effect size differed between groups.
Ninety-five per cent confidence limits around mean effect
sizes were obtained by bootstrapping (bias corrected
confidence limits based on 4999 iterations; cf. Adams
et al. 1997). An effect is statistically significant if its
confidence intervals do not overlap with zero. Following
conventional practice, the size of a mean effect size was
considered small when less than 0.2, moderate when 0.5
and large when greater than 0.8 (Gurevitch & Hedges
1993).
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388 S. Gripenberg et al.

Review and Synthesis

All analyses were performed in MetaWin version 2


(Rosenberg et al. 2000). Studies included in the analyses are
listed in Appendix S3.
RESULTS

The data compiled allowed us to compare the relationship


between female preference and offspring performance on
2129 pairs of plant types, depending on the response
(Appendix S3). Visual exploration of the data revealed no
signs of publication bias (Fig. 1): setting aside
some extreme outliers (notably in Fig. 1c), the variation
around the overall effect size decreased with sample size,
effect sizes were independent of sample size, and at any
given sample size, individual studies were normally
distributed around the overall effect size (cf. Rosenberg
et al. 2000).
The majority of studies in our data base concern
Lepidoptera, with scattered entries of studies involving
other insect orders (Appendix S3). Effect sizes did not
differ significantly between insect orders (Table 2), although
in the preference data QB was almost significant (P = 0.06).
This pattern was mainly due to the small effect sizes
observed in two studies on Hemiptera (Fig. 2). Based on
these results, we conclude that pooling data from studies
conducted on different insect groups is unlikely to have
biased our results.

Overall support for the bitrophic PPH (Hypothesis H1)

The summary analyses provide clear support for a link


between female preference and offspring performance (i.e.
for Hypothesis H1 in Table 1). Overall, offspring were
more likely to survive on plant types prefered by ovipositing
females. Likewise, the number of eggs laid by females was
higher on plants on which offspring perform well (Fig. 3).
There was also a trend for offspring to be larger and to
develop faster on plant types preferred by ovipositing
females, although for these performance traits the overall
effect sizes did not differ significantly from zero (Fig. 3).
Where significant, the mean effect sizes in the models
without any data structure were 0.73 (preference) and 0.95
(survival), and were hence moderate to large (Gurevitch &
Hedges 1993). For all response variables, except for
offspring survival, the total heterogeneity of effect sizes
(QT) was statistically significant when tested against a v2
distribution with appropriate degrees of freedom (Table 2),
indicating that the variance in effect sizes was greater than
could be explained by sampling error alone.
Ecological and life history modifiers of the preference
performance relationship (Hypothesis H2)

As the distribution of effect sizes revealed no sign


of unexplained variation around joint mean survival

(a) 4

(b) 6

0 20 40 60 80 100 120 140 160 180 200


n

(c)

50

100

150

200

250

(d) 5

3
2

lnOR

1
0

1
2
3

2
0 100 200 300 400 500 600 700 800 900
n

3
0

10 20 30 40 50 200
n

250

Figure 1 Funnel plots showing relationships between effect size (Hedges d or ln OR) and sample size in the analyses of offspring (a) weight,

(b) development time, (c) survival and (d) female preference. In panels ac, sample sizes (n) refer to the number of individuals used
to measure performance on the plant type preferred by females (in most studies, sample sizes on the less preferred plant are similar). In panel
d, n shows the number of units (typically individuals) of good quality plants on which oviposition was assessed.
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Review and Synthesis

Preferenceperformance in insects 389

Table 2 Total heterogeneity (QT) and between-group heterogeneity (QB) of effect sizes in studies comparing offspring weight, development
time, and survival on preferred and less preferred plant types, and female preference (i.e. no. eggs laid) for good versus poor quality hosts. QT
values are given for models without data structure (i.e. no explanatory variables). As QT was non-significant in the summary analysis on
survival, no further explanatory factors were examined for this response.

Response

Grouping variable

QT

Weight

QB

51.83
Insect order
Diet specialization
Woody or non-woody plant
Offspring mobility
Egg distribution
Feeding by adults
Inter- or intraspecific study

Development time

1.55
0.98
0.18
0.62
0.01
2.26
0.05
77.27

Insect order
Diet specialization
Woody or non-woody plant
Offspring mobility
Egg distribution
Feeding by adults
Inter- or intraspecific study
Survival
Preference

3.09
0.14

0.003
0.22
0.20
0.02
18.90
53.68

Insect order
Diet specialization
Woody or non-woody plant
Offspring mobility
Egg distribution
Feeding by adults
Inter- or intraspecific study

2.4

8.85
14.83
0.51
1.13
0.24
0.04
0.59

n=3

1.0

0.4
n=2

0.4

Effect size

Effect size

0.003
0.46
0.61
0.67
0.43
0.91
0.13
0.83
< 0.00001
0.21
0.93

0.95
0.64
0.65
0.90
0.53
0.002
0.06
0.0006
0.55
0.29
0.62
0.83
0.43

n = 29

n=4

0.8

0.0

27
2
2
1
1
1
1
1
21
2
2

1
1
1
1
20
28
4
2
1
1
1
1
1

n = 21

1.5

n = 10

1.2

2.0

n = 10

2.0
1.6

d.f.

0.5

n = 28
n = 22

0.0
0.5

0.8
1.2

1.0

1.6
1.5

2.0
2.4

2.0

Diptera

Lepidoptera Hymenoptera Coleoptera Hemiptera

Weight Development time Survival

Preference

Figure 2 Mean effect sizes (with 95% bias corrected confidence

Figure 3 Overall effect sizes for the four response variables

intervals) for studies conducted on different insect orders in the


preference analysis.

addressed in this study. For offspring weight and development


time, and for female choice, the effect size used is Hedges d; for
offspring survival, it is ln(OR). Bars are 95% bias-corrected
confidence limits. Where confidence limits do not overlap with
zero (grey line), effect sizes are considered statistically significant.

(non-significant QT, Table 2), we dropped this response


variable from our analyses of ecological and life-history
factors influencing the preferenceperformance relation-

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390 S. Gripenberg et al.

(a)

Review and Synthesis

n =11

2.5

(b) 1.6

n = 17

2.0

Effect size

n = 10

n = 17 n = 7

1.0

n=6

n = 11

n=7

0.5
n=2

0.0

0.4

0.5

1.5
2.0
2.5

(c)

0.0
0.4

Monophagous
Oligophagous
Polyphagous

Woody plants
Nonwoody plants

0.8

Weight

Development time

Weight

Preference

2.0

n = 19

1.0

n =16
n=6

0.0

0.5

0.5

1.0

1.0
1.5

Free-feeding
Sessile

n = 14
n=8

Batches
Single eggs

2.0

2.0

Weight

Development time

Preference

Weight

Development time

Preference

(f)

2.0

2.0
n=8

n=7

1.5

n = 21

1.0

n = 20 n = 9

1.5
1.0

n = 21

n = 18

n = 12
n = 10

n = 20

0.5

0.5

n=2

0.0

0.0

0.5

0.5

1.0

1.0

1.5

n = 13

n = 14 n = 14

0.5

0.0

(e)

n = 16

1.5
n = 15

0.5

1.5

Preference

n = 14
n=9

1.0

Development time

(d) 2.0

1.5

Effect size

n = 22

0.8

n = 10

n=4

1.0

Effect size

n = 12

1.2

1.5

1.5

Feeding by adults
Adults do not feed

2.0

n = 10

Interspecific
Intraspecific

2.0

Weight

Development time

Preference

Weight

Development time

Preference

Figure 4 Mean effect sizes (with 95% bias corrected confidence intervals) for studies grouped according to explanatory variables. In each

panel, the results from analyses of each response variable (weight, development time, female preference) are displayed. The different panels
show the effect of (a) diet specialization (P2.1 in Table 1), (b) type of host (i.e. woody or herbaceous; P2.2), (c) offspring mobility (P2.3), (d)
pattern of egg distribution (P2.4), (e) feeding by adults (P2.5) and (f) whether the study assessed the preferenceperformance relationship
inter- or intraspecifically (P2.6). All but one study in our data set on development time was conducted on non-woody plant species,
preventing us from examining the effect of this explanatory variable on this particular response.

ship. For the other response variables, most of the


explanatory factors examined (Table 1; P2.1P2.6) had no
detectable influence on the link between preference
and performance (Table 2, Fig. 4). However, when
insects were grouped according to their degree of diet
specialization, effect sizes differed significantly between
groups in the preference analysis (Table 2, Fig. 4a). Here,
 2010 Blackwell Publishing Ltd/CNRS

the mean effect size was larger for studies conducted


on oligophages than for studies conducted on polyphages
or monophages (Fig. 4a). In other words, the link
between female preference and offspring performance
was stronger for insects specialized on plants within a
certain family than for insects with either broader or
narrower diets.

Review and Synthesis

DISCUSSION

This study provides a first quantitative synthesis of evidence


pertinent to the preferenceperformance relationship in
herbivorous insects. For both performance (survival) and
preference, overall effect sizes were moderate to strong
(Gurevitch & Hedges 1993) and significantly differed from
zero (Fig. 3). As all data points in our meta-analysis
emanated from studies conducted in isolation from natural
enemies, competitors and mutualists, this study can be seen
as offering unequivocal support for the preferenceperformance hypothesis in a bitrophic setting. Given the effort
taken to explain situations where female choice does not
match patterns of offspring performance (e.g. Thompson
1988; Courtney & Kibota 1990; Mayhew 1997; Craig &
Itami 2008), this is in itself a remarkable result. Compared
with previous narrative reviews of the topic, this study then
illustrates the advantage of quantitative research synthesis as
a way of seeing the wood for the trees. Although there are
convincing examples of cases where female choice does not
match offspring performance (e.g. Rausher 1979; Valladares
& Lawton 1991; Underwood 1994; Fritz et al. 2000; Faria &
Fernandes 2001 and examples in Appendix S3), the
general rule is clearly a positive association be it with
modifications.
Based on the information available in our data base, we
were able to test six specific factors proposed to influence
the strength of the preferenceperformance relationships.
Of these, the current data provide support only for a role of
diet breadth: In the preference analyses, effect sizes were
larger for oligophagous than for polyphagous insects. This
pattern supports the neural constraints hypothesis (e.g.
Bernays 1998; Bernays & Funk 1999; Janz 2003), which
posits that the behaviour of insects may be constrained by
the limitations of their neural system to process complex
information. It is equally compatible with the idea that
specialization may allow fine-tuning to the characteristics
of individual host species although multiple physiological
and morphological means (e.g. Roslin & Salminen 2008). In
such a case, the relationship between diet breadth and the
accuracy of female choice might not necessarily be due to
non-adaptive constraints, but could also suggest that
oligophages are under stronger selection to develop a
preference for high quality plants than are insects with
broader diets. Nevertheless, the observed pattern came with
a curious twist: effect sizes for monophages were significantly smaller than for oligophages (and approximately the
same size as for polyphages), suggesting that the preference
performance link may be strongest for insects with an
intermediate level of diet specialization. The comparably
weak preferenceperformance relationship observed in
monophages may be a methodological artefact. Clearly,
plants belonging to different genera and families are likely to

Preferenceperformance in insects 391

differ in more ways than are plants of the same species. As


monophages were defined as insects specialized on plants
within a genus, the plant types in plant pairs on which the
preferenceperformance relationship is assessed will likely
be more similar than is the case in studies on oligophagous
and polyphagous insects. In studies conducted on monophagous insects, 100% of the data points involve comparisons
on plants belonging to the same species or the same genus,
whereas the corresponding figure for oligo- and polyphagous insects was 4554%, depending on the response. At
this point, we consider this the most plausible explanation
for the observed pattern.
Of the five other predicitions tested, none gained
support. Whether these negative results reflect true patterns
or whether they are partly due to the lack of statistical power
remains open to debate but at this point, this study does
not back them up as major modifiers of the general
relationship between preference and performance. Instead,
among the wealth of specific hypotheses put forward to
account for variation in the strength of preference
performance coupling, this study pinpoints diet breadth as
a promising avenue for future research.
While the patterns discussed above serve to bring out the
advantages of meta-analysis, there are also limits to this
approach the most important of which are due to the
motley methodology and style of reporting which is
common in PPH research. From a practical perspective,
the variable approaches taken to measure the link between
preference and performance as well as in presenting the
results makes it challenging to combine data from different
studies. Consequently, only a fraction of the studies
conducted to date could be included in our meta-analyses.
Compared with the general volume of studies conducted in
this field (see Data generation), the set of n = 2129 useful
studies identified by us per response will seem vanishingly
small (Appendix S3). Moreover, data to test additional
factors proposed to influence the strength of the preferenceperformance relationship such as the effect of time
limitation (e.g. Ward 1987), phylogenetic constraints (e.g.
Price 1994, 2003) and the co-evolutionary history of the
plantinsect associations tested (e.g. Agosta 2006) are not
readily available. As a result, there are currently limits to the
kind of questions that can be answered by means of metaanalysis. Hence, we urge our colleagues to continue
addressing the many intriguing questions flourishing within
the subject field and when reporting the fruits of their
work, to present their data in a coherent format. Most
importantly, they should remember to include at least
group-specific means, sample sizes and standard deviations
a recommendation which may seem trivial, but is rarely
met. To stimulate this development, we will continue
building on the data base we have now established
(Appendix S3), with the aim of eventually addressing new
 2010 Blackwell Publishing Ltd/CNRS

392 S. Gripenberg et al.

questions with additional data, and exposing old ones to the


critical test of additional data. We believe that such a
compilation of data will be helpful in advancing the field,
and invite our colleagues to join in on the effort by
communicating their quantitative findings to us.
ACKNOWLEDGEMENTS

We thank all authors that have responded to our queries on


specific details on individual study systems, and the
following people for sharing their expertise on particular
insect taxa: Anders Albrecht, Heikki Roininen, Marko
Mutanen, Soren Nylin and Stig Larsson. Bob OHara
provided statistical advice and three anonymous referees
offered valuable suggestions for improvement. Financial
support from the Academy of Finland (grant number
129636 to the Centre of Excellence in Metapopulation
Research 2009-2011, and grant numbers 126296 and 129142
to SG and TR, respectively), and from the Ella and Georg
Ehrnrooth foundation (to SG) is gratefully acknowledged.
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SUPPORTING INFORMATION

Additional Supporting Information may be found in the


online version of this article.
Appendix S1 Ranking of plant types.
Appendix S2 Criteria used in pruning non-independent data

points.
Appendix S3 Studies included in the meta-analyses.

As a service to our authors and readers, this journal provides


supporting information supplied by the authors. Such
materials are peer-reviewed and may be re-organized for
online delivery, but are not copy-edited or typeset. Technical
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than missing files) should be addressed to the authors.

Editor, John Jaenike


Manuscript received 27 October 2009
First decision made 23 November 2009
Manuscript accepted 1 December 2009

 2010 Blackwell Publishing Ltd/CNRS