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R E S E A R C H Open Access
Food load manipulation ability shapes flight
morphology in females of central-place
foraging Hymenoptera
Carlo Polidori
1*
, Angelica Crottini
2
, Lidia Della Venezia
3,5
, Jesús Selfa
4
, Nicola Saino
5
and Diego Rubolini
5
Abstract
Background: Ecological constraints related to foraging are expected to affect the evolution of morphological traits
relevant to food capture, manipulation and transport. Females of central-place foraging Hymenoptera vary in their
food load manipulation ability. Bees and social wasps modulate the amount of food taken per foraging trip
(in terms of e.g. number of pollen grains or parts of prey), while solitary wasps carry exclusively entire prey items.
We hypothesized that the foraging constraints acting on females of the latter species, imposed by the upper limit
to the load size they are able to transport in flight, should promote the evolution of a greater load-lifting capacity
and manoeuvrability, specifically in terms of greater flight muscle to body mass ratio and lower wing loading.
Results: Our comparative study of 28 species confirms that, accounting for shared ancestry, female flight muscle
ratio was significantly higher and wing loading lower in species taking entire prey compared to those that are able
to modulate load size. Body mass had no effect on flight muscle ratio, though it strongly and negatively co-varied
with wing loading. Across species, flight muscle ratio and wing loading were negatively correlated, suggesting
coevolution of these traits.
Conclusions: Natural selection has led to the coevolution of resource load manipulation ability and morphological
traits affecting flying ability with additional loads in females of central-place foraging Hymenoptera. Release from
load-carrying constraints related to foraging, which took place with the evolution of food load manipulation ability,
has selected against the maintenance of a powerful flight apparatus. This could be the case since investment in
flight muscles may have to be traded against other life-history traits, such as reproductive investment.
Keywords: Bees, Flight Muscle Ratio, Foraging, Wasps, Wing Loading
Introduction
Flying animals show a huge diversity of body shapes and
structures and, as a consequence, a great variation in
flight performance that in turn largely affects the ability
to avoid predators, chase mates and carry food items
[1-4]. An intriguing question is thus whether variation
in flight morphology is adaptively tuned to specific eco-
logical conditions, such as habitat type, or to specific be-
havioural traits, such as food preferences [5]. Flying
animals must generate a lift force sufficient to counter-
act the gravitational force acting on their bodies, and
this requirement is frequently exacerbated when an
additional load has to be carried in flight, which com-
monly occurs during foraging [6,7]. Load-lifting and
manoeuvrability limits may constrain foraging and entail
important ecological and evolutionary consequences.
Based on previous theoretical and empirical studies it
is possible to make predictions about the relationship
between morphology, lift production, power output and
take-off ability. Experiments on insects, birds and bats
have revealed that flight muscle ratio (i.e., the flight
muscle mass to body mass ratio, FMR) is the most im-
portant determinant of take-off ability with additional
loads [6]. Because flying animals generate an approxi-
mately constant force per unit of flight muscle during
high-intensity bursts of flight [6], FMR also affects,
together with other morphological traits (e.g. position
of center of body mass), acceleration and, partly,
* Correspondence: cpolidori@mncn.csic.es
1
Departamento de Biodiversidad y Biología Evolutiva, Museo Nacional de
Ciencias Naturales (CSIC), C/ José Gutiérrez Abascal 2, 28006 Madrid, Spain
Full list of author information is available at the end of the article
© 2013 Polidori et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative
Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and
reproduction in any medium, provided the original work is properly cited.
Polidori et al. Frontiers in Zoology 2013, 10:36
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manoeuvrability in flight (since it could be considered as
a series of changes in acceleration) [1,2]. Furthermore,
relatively larger wings compared to body size, corre-
sponding to a lower wing loading (WL) (i.e., the body
mass to wing area ratio) are also associated with a super-
ior flying ability [2,8]. Animals with lower WL can per-
form a more energetically efficient flight [9,10] and take
off at higher speed (though cruising flight speed in-
creases with WL [11]).
Studies of insects have shown that intraspecific vari-
ation in flight morphology also has important fitness
consequences: for example, higher FMR in males has
been related to a better competitive ability in territorial
wasps [12] and dragonflies [1,13]. In a pompilid wasp,
competitively successful males are larger, with a ten-
dency for reduced WL [3]. Comparative studies are
scarce, but still suggest the same patterns. For example,
ant-attended aphid species have higher WL and smaller
amount of flight muscles (implying a lower dispersal
ability) than non-ant-attended species [14,15]. Similarly,
palatable and non-mimetic butterflies have higher FMR,
enhancing their escape ability [2]. Interestingly, in both
aphids and butterflies, species with reduced flight thorax
muscle mass allocate more resources to reproduction
(e.g. ovarian size) [2,14,15], suggesting a trade-off be-
tween investment in flight muscles and reproduction.
On the whole, these studies indicate that flight morph-
ology in insects is shaped by multiple, potentially con-
trasting selection pressures, including the ability to
defend a territory and the ability to escape from preda-
tors, though other sources of selection have not yet been
investigated. In particular, despite the known role of for-
aging behaviour and diet type in shaping the flight
morphology of predatory vertebrates [8,16], to the best
of our knowledge no study has examined these evolu-
tionary relationships among predatory insects.
Flying, central-place foraging Hymenoptera (Aculeata),
whose females repeatedly return with a food load to
their nest in order to provision their immature brood,
are an excellent system to study the evolutionary rela-
tionships between foraging ecology and flight morph-
ology. This diverse group includes bees and wasps and
shows huge variation in foraging ecology, as it includes
predators hunting arthropods or other animal sources as
well as pollen/nectar foragers [17]. Importantly, central-
place foraging aculeates vary markedly in their foraging
mode: some species, such as bees and social vespid
wasps, have evolved the ability to modify the shape and
size of food material and thereby the load carried in
flight before transporting it to the nest. Bees can tune
pollen and nectar load, whereas social vespid wasps
often divide large prey in pieces and carry only parts of
them on each foraging trip [18,19] (here defined as “able
to manipulate”species, AtM species hereafter). In
contrast, solitary vespid wasps and apoid wasps can only
hunt and carry entire prey items to provision their
brood. These species (here defined as “unable to ma-
nipulate”species, UtM species hereafter) should thus se-
lect prey weighing less than or equal to the maximum
load they can carry in flight [7]. Because wasps able to
divide in pieces large prey can successfully return by fly-
ing to the nest with food [20], while wasps unable to do
this, in the same condition, often fail to forage (though
in certain species females would shift to prey dragging
over the ground [7]), we hypothesized that inability to
modulate load size, rather than the type of food con-
sumed (prey or pollen), should impose foraging con-
straints to UtM species, and that such constraints
should lead to the evolution of a flight morphology that
maximizes the ability to carry heavier loads.
UtM species are predicted to have therefore evolved a
higher FMR and a lower WL, unless investment in flight
muscles and wing size is counteracted by contrasting se-
lection on other life-history traits, such as reproductive
investment. Here we tested the prediction that variation
in FMR and WL is associated with food load manipula-
tion ability in central-place foraging Hymenoptera, with
UtM species expected to have higher FMR and lower
WL than AtM species. Furthermore, across species, we
also expected these traits relevant to flight performance
to have coevolved, with species having high FMR also
having a lower WL.
Results
The identification of the ancestral state on the recon-
structed phylogeny revealed that food manipulation ability
is a derived trait for both Apoidea and Vespoidea, with the
more primitive species all being unable to manipulate load
size (Figure 1). Furthermore, character mapping revealed
that food manipulation ability has independently evolved
twice in this set of Hymenoptera species, once in Apoidea
and the other in Vespoidea (Figure 1).
Our species’sample encompassed a huge range of body
masses (M
b
), from very small species weighing < 0.01 g to
very large ones weighing 0.85 g (Table 1). After controlling
for phylogeny and body mass, food load manipulation sig-
nificantly predicted FMR (Table 2). Specifically, AtM-
species had smaller FMR than UtM ones (Table 1 and
Table 2, Figure 2). Body mass did not covary with FMR,
and the estimated value of λindicated that FMR showed
almost no phylogenetic dependence (LR test, P = 0.99)
(Table 2), suggesting that phylogenetic constraints did not
affect the evolution of FMR in this species’set.
The maximum food load that could be theoretically
carried in flight by a species (Load
max
) was estimated to
range from 0.007 g to over 0.7 g (0.14 ± 0.01 g on
average) (Additional file 1: Table S2). The total load that
could be lifted (M
max
= Load
max
+M
b
) ranged from
Polidori et al. Frontiers in Zoology 2013, 10:36 Page 2 of 11
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0.015 g to 1.55 g. In turn, UtM-species were predicted to
carry loads weighing 118 ± 0.06% of their body mass,
while this value was reduced to 86 ± 0.06% of body mass
in AtM-species (Additional file 1: Table S2).
Wing size (A
w
) was also very variable among species,
with values ranging from less than 0.1 cm
2
to > 2 cm
2
(Additional file 1: Table S2). WL was smaller in UtM-
species compared to AtM ones, after controlling for phyl-
ogeny and body mass (Table 2, Figure 2). In this model,
body mass strongly positively covaried with WL (Table 2)
(see also Materials and methods), and the degree of phylo-
genetic dependence was relatively large (0.70, Table 2) and
statistically significant (LR test, P = 0.011), Thus, differ-
ently from FMR, WL showed a high degree of phylogen-
etic autocorrelation, with closely related species showing
more similar WL values than distantly related ones.
Results concerning the effect of food manipulation
ability on FMR and WL were qualitatively unaltered if
we used FMR and WL values based on dry mass (see
Materials and methods) and head width instead of body
mass as a covariate, despite the smaller sample of 21
species (Additional file 1: Table S3).
Since in our database all UtM species were arthropod
predators, and most AtM species were pollen/nectar
feeders (the exception were the few social vespid wasps),
the strict association between dietary specialization
(pollen/nectar vs. animal proteins) and food load manipu-
lation ability may have confounded the above results. We
therefore conducted an additional analysis of the effect of
food manipulation ability on flight traits by excluding all
the pollen/nectar feeders (i.e., bees) and restricting the
dataset to wasps (including both UtM species, n = 14, and
AtM species, n = 4). The analysis was conducted only on
FMR, since sample size for WL was too small (only 2 AtM
species). Despite the small sample size, the results con-
firmed the previous analyses, with significantly smaller
FMR in the few AtM (0.364 ± 0.008) compared to the
UtM species (0.407 ± 0.01) (PGLS model accounting for
heterogeneity of variances and body mass; effect of food
manipulation ability: -0.036 ± 0.017, t
15
= 2.15, P = 0.048,
λ= 0.26; further details not shown for brevity).
The covariation between WL and FMR across species
was negative and statistically significant (PGLS model ac-
counting for body mass, FMR estimate: -1.27 ± 0.42,
t
20
=−3.03, P = 0.007, λ= 0.82; body mass estimate 0.34 ±
0.05, t
20
= 6.43, P < 0.001) (Figure 3).
Discussion
We showed that the evolution of food load manipulation
ability, which has occurred independently twice in the
Figure 1 Partitioned Bayesian tree based on a 50% majority rule consensus tree from the analysis of 1433 bp of the 18S rRNA and 28S
rRNA gene fragments sequences of the selected Hymenoptera taxa. Scolebythus madecassus was used as an outgroup. Asterisks denote
Bayesian posterior probabilities values: *, 95–98%; **, 99–100%. Maximum Likelihood Markov model (Mk1) ancestral state reconstruction
describing the food load manipulation ability on the MrBayes topology: AtM (“able to manipulate”species, names in grey) vs. UtM (“unable to
manipulate”species, names in black). Pie diagrams at each node indicate the proportion of the Maximum Likelihood supporting alternative
reconstructed character states. Bars define Families and Superfamilies. Species names refer to the sample used to build the phylogenetic tree; for
correspondence with the morphologically studied species, see Additional file 1: Table S2. Pictures show, from top to down, Polistes sp. (Vespidae)
at nest, Ammophila sp. (Sphecidae) with prey and Bombus sp. foraging on flowers (Apidae).
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Table 1 Dataset used for comparative analyses, including wet body mass (M
b
), flight muscle ratio (FMR), wing loading (WL), dietary specialization (pollen/
nectar or animal protein) and food manipulation ability (0 = unable to manipulate food load, 1 = able to manipulate food load)
Taxonomy Species Species used in the phylogenetic reconstruction Diet Food manipulation ability M
b
(g) FMR WL (g/cm
2
) Source
Apoidea: Apidae Amegilla dawsoni Amegilla asserta Pollen 1 0.700 - 0.31 [21]
Apoidea: Apidae Anthophora sp. Anthophora montana Pollen 1 0.133 0.396 0.183 This study
Apoidea: Apidae Apis mellifera Apis mellifera Pollen 1 0.094 0.358 0.170 This study
Apoidea: Apidae Bombus impatiens Bombus diversus Pollen 1 0.201 0.261 0.287 [22]
Apoidea: Apidae Bombus sp. 1 Bombus ardens Pollen 1 0.208 0.374 0.220 This study
Apoidea: Apidae Bombus sp. 2 Bombus mendax Pollen 1 0.204 0.401 0.199 This study
Apoidea: Apidae Xylocopa varipuncta Xylocopa pubescens Pollen 1 0.838 0.342 0.331 [23]
Apoidea: Megachilidae Anthidium manicatum Anthidium porterae Pollen 1 0.154 0.344 0.205 This study
Apoidea: Megachilidae Megachile rotundata Megachile pugnata Pollen 1 0.102 0.32 0.178 This study
Apoidea: Megachilidae Osmia rufa Osmia lignaria Pollen 1 0.187 0.353 0.223 This study
Apoidea: Sphecidae Ammophila sabulosa Ammophila sp. JC134 Prey 0 0.026 0.409 0.075 This study
Apoidea: Sphecidae Sceliphron curvatum Sceliphron caementarium Prey 0 0.083 0.46 0.094 This study
Apoidea: Sphecidae Sceliphron destillatorium Sceliphron laetum Prey 0 0.181 0.44 0.124 This study
Apoidea: Sphecidae Sphex rufocinctus Sphex lucae Prey 0 0.118 0.426 0.109 This study
Apoidea: Crabronidae Bembix olivacea Bembix americana Prey 0 0.109 0.46 0.122 This study
Apoidea: Crabronidae Bembix sinuata Bembix dentilabris Prey 0 0.158 0.456 0.195 This study
Apoidea: Crabronidae Bembix troglodytes Bembix amoena Prey 0 0.099 0.36 - [24]
Apoidea: Crabronidae Oxybelus sp. Oxybelus abdominalis Prey 0 0.008 0.374 0.087 This study
Apoidea: Crabronidae Philanthus pulchellus Philanthus gibbosus Prey 0 0.043 0.392 0.08 This study
Apoidea: Crabronidae Philanthus triangulum Philanthus sp. CSM-2006 Prey 0 0.092 0.401 0.116 This study
Vespoidea: Vespidae Polistes dominulus Polistes metricus Prey 1 0.065 0.369 0.085 This study
Vespoidea: Vespidae Vespula germanica Vespula germanica Prey 1 0.067 0.361 - [20]
Vespoidea: Vespidae Vespula maculifrons Vespula maculifrons Prey 1 0.038 0.381 - [20]
Vespoidea: Vespidae Vespula vulgaris Vespula squamosa Prey 1 0.078 0.344 0.139 This study
Vespoidea: Vespidae Eumenes sp. 1 Eumenes fraternus Prey 0 0.048 0.403 0.078 This study
Vespoidea: Vespidae Eumenes sp. 2 Eumenes tripunctatus Prey 0 0.042 0.375 0.098 This study
Vespoidea: Vespidae Euodynerus sp. Euodynerus megaera Prey 0 0.049 0.363 0.067 This study
Vespoidea: Vespidae Monobia quandridens Monobia quandridens Prey 0 0.218 0.385 - [25]
Polidori et al. Frontiers in Zoology 2013, 10:36 Page 4 of 11
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present set of species, is associated with a decrease of
FMR and an increase in WL across species. Moreover, a
high FMR was associated with a low WL, indicating
coevolution of morphological traits related to foraging.
Within, as well as across, wasp species, the depend-
ence of the maximum theoretical load that could be car-
ried (Load
max
) on body mass allows larger individuals/
species to potentially carry large prey, even though there
is no relationship between FMR and body mass (Table 2).
Empirical studies of individual wasp species indeed
showed that larger individuals carry larger prey com-
pared to smaller ones [20,25,26]. Moreover, larger spe-
cies appear to be able to carry heavier loads (Pearson
correlation test, r = 0.95, P < 0.001, data from 12 species
reviewed by [7]). However, the degree to which individ-
uals and species maximize their food load is highly
variable, suggesting that other factors, such as prey
specialization [27], prey availability [28] and intra-
specific competition [24] may affect the food load mass.
For example, females of Bembix troglodytes, a solitary
wasp of about 0.01 g, hunt for flies weighing only half
the theoretical maximum they can carry [24]. This may
be a strategy to limit the attack of conspecific klepto-
parasitic females, since carrying small prey may allow
entering nest holes more rapidly and avoiding harass-
ment [24]. On the other hand, the species-specialist
cicada-hunting wasp Sphecius convallis carries prey
loads approaching the theoretical maximum value of
Load
max
, possibly because the strong specialization on a
single prey species has allowed selection to adjust the
morphology of females to an almost ideal size [27].
As re-calculated from data provided in a recent review
[7], UtM-species carry on average loads weighing 89 ±
14% of body mass (data from 11 species of Sphecidae,
Crabronidae and Vespidae), similar to the predicted
% Load
max
/M
b
average value of 118% on the entire set of
species considered in this study (89.3% with data for the
shared UtM-species in our study and [7], n = 7 species).
Moreover, among UtM species, there was no correlation
between prey size and FMR (Pearson correlation test,
r = 0.43, P = 0.19, data from 11 species reviewed by [7]).
It is believed that the first apoid wasps were specialized
in hunting large orthopterans, and the prey spectrum
would have then become broader to include smaller
Table 2 PGLS models testing the effect of food load
manipulation ability (0 = UtM; 1 = AtM) on flight muscle
ratio (FMR) and (log
10
-transformed) wing-loading (WL),
while controlling for wet body mass (log
10
-transformed)
Model Estimate (s.e.) t P λ
FMR (n=27 species)
Food load manipulation ability −0.059 (0.016) −3.71 0.001 0.01
Body mass 0.013 (0.021) 0.64 0.53
WL (n=24 species)
Food load manipulation ability 0.148 (0.059) 2.49 0.021 0.70
Body mass 0.278 (0.053) 5.25 < 0.001
The maximum likelihood estimate value of λ, assessing the degree of
phylogenetic dependence among the tested variables (see Materials and
methods), is shown for each model.
Figure 2 Box-and-whisker plots of flight muscle ratio and wing
loading in relation to food load manipulation ability. a flight
muscle ratio (FMR). bwing loading (WL). Medians (horizontal lines
within boxes), means (■), 1º and 3º quartile (top and bottom
horizontal lines of the boxes), as well as maximum and minimum
values (○) are shown for the species able to manipulate the food
load (AtM-species) and for the species unable to manipulate the
food load (UtM). Endpoints of the whiskers represent the lowest
datum still within 1.5 × interquartile range of the lower quartile,
and the highest datum still within 1.5 × interquartile range of the
upper quartile.
Figure 3 Relationship between of WL and FMR. The correlation is
based on a total of 23 species, i.e. those for which both variables
were available.
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arthropods as diverse as flies, bees, beetles and spiders
[29]. Thus, the evolution of flight morphology adapted
to carry large items possibly preceded, during evolution,
prey diversification, and did not change too much there-
after in apoid wasps. A change in flight morphology may
have appeared when bees (sensu stricto, i.e. pollen/nectar
foragers) separated from apoid wasps about 140 to 110
m.y.a. [30]. A similar pattern may have occurred among
Vespidae, where solitary species (subfamily Eumeninae),
unable to manipulate food load size, are basal to the so-
cial species [31], which are able to manipulate food. In
Eumeninae, prey diversification was less pronounced,
with only lepidopteran or coleopteran larvae used as
prey, and a change in flight morphology may have
appeared when eusociality, together with its associated
foraging mode (e.g. direct liquid-feeding from adult for-
agers to larvae, made possible because of food manipula-
tion ability) evolved [32].
The maintenance of higher FMR in UtM-species could
also depend on the fact that the position of load during
carrying may affect the center of gravity, unbalancing
the wasp while flying. A recently developed model shows
that, among species carrying prey impaled on the sting
(i.e. well posterior to the wasp center of gravity), the
Load
max
can be severely reduced compared to the
expected value [33]. Wasps can limit to some extent this
problem by increasing the angle which the straight line
connecting the wasp with the load center of mass makes
with the horizontal line [33], but, evolutionarily speak-
ing, any increase in FMR, positively affecting Load
max
,
would help in carrying larger prey in such an unbalanced
flight mode.
On the other hand, AtM species are far from ap-
proaching the average values of relative load size ob-
served among UtM species, as they appear carrying
loads weighing only 31 ± 6% (calculated from data of 17
species provided in [20,34-36]). This value is much lower
than the average % Load
max
estimated for our set of
AtM-species (86%).
Actually, females of UtM-species were sometimes ob-
served to return to the nests with a prey weighing more
than Load
max
, implying an unsuccessful take-off [7].
With very large prey items, UtM wasps can potentially
shift to an alternative strategy, such as carrying the prey
to the nest by dragging it on the ground. Such behaviour
has been described in some (but not all) species, though
flight transportation was the preferred option if prey size
is adequate [7]. For example, Ammophila spp. typically
drag large caterpillar prey over the ground, but shift to
flight transportation in case of smaller prey (reviewed in
[37]). Indeed, dragging a prey on the ground may make
it much more vulnerable to kleptoparasites and preda-
tors. The cicada-hunting wasp Sphecius speciosus can
drag very large cicadas over a distance sometimes full of
obstacles (e.g. dense and high grass) which makes prey
prone to be abandoned and exploited by ants [7]. Drag-
ging a prey over such complex substrates may also in-
crease the duration of the hunting trip compared to
flying across the same distance. Despite hunting site-
nest distances are not provided and conclusions cannot
be really drawn, data from the literature reported very
short hunting trips (≤2 minutes) apparently only for
flight-carrying wasps (e.g. [38-41]). Thus, although in
specific cases wasps can use the alternative strategy of
dragging very large prey, we expect a fitness advantage
in term of foraging efficiency (e.g. number of prey
hunted per day) when the prey is carried in flight.
Clearly, a robust and direct comparison of the actual fit-
ness costs and benefits of prey carrying in flight vs. prey
dragging would be needed to confirm this speculation.
An interesting consequence of load-lifting/manoeuvrability
constraints concerns diet composition and resource speciali-
zation. In bees, any individual could have access to its pre-
ferred resource (assuming these are available in the foraging
environment) because food collection is only limited by the
number of pollen grains it can carry and by the nectar
volume it can ingest, i.e. by volumetric, not mass, con-
straints.Inwaspsthatareabletomanipulatefoodloadthe
situation is similar: Coelho and Hoagland [20] studied the
foraging behaviour of Vespula germanica on dead honey-
bees, and found that foragers too small to carry entire
honeybees simply chopped body parts and took off with a
smaller portion [20], without the need to discard the food
item and search for a new, smaller one. Food manipulation
ability would thus help to exploit the target food in a highly
efficient way. At the same time, AtM-wasps can have access
to a wider range of prey types, since also large prey, once
chopped, can be readily exploited. Such increased efficiency
in foraging may have even been important in promoting the
evolution of eusociality, since social behaviour is unstable
unless it provides important economic benefits and fitness
gains to the individuals [42]. As a matter of fact, eusociality
arose at least five times independently within AtM-lineages,
while apparently only once within UtM-lineages (see also
[43,44] for theoretical predictions on the link between food
resource and social evolution in Hymenoptera).
On the other side, wasp species unable to manipulate
food load will face a more adverse situation if the prey
item is too large to be carried, and the wasp has to
spend additional time and energy to search for a differ-
ent, smaller, profitable prey [7]. In a simple model,
Polidori et al. [45] predicted that wasp species hunting
for hemimetabolous prey can be so affected by the body
growth of their preferred prey during the course of the
breeding season that they may be forced to shift to dif-
ferent prey species at a certain point. Later, a study on
the orthopteran-hunting wasp, Stizus continuus, con-
firmed this prediction [46]. Furthermore, this shift to
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smaller prey species is confined in such wasps to only
few other species, given their phylogenetic constraint in
prey selection (typically prey species belong to one single
order [17]), so that overall prey spectrum cannot be wide
as in AtM-wasps.
As an additional advantage, higher FMR would enhance
the escape ability of UtM-species, given that FMR is corre-
lated with linear acceleration and the ability to accelerate
vertically against gravity [2] and with flight speed [47].
Low WL is expected to confer similar advantages. In
UtM-wasps, which are also those limited to hunt for living
prey, lower WL could increase manoeuvrability during
prey transportation, but could also increase efficiency
while pursuing a living prey (e.g. via reduced minimum
flight-speed requirement and turning radius), including
fast-flying insects [48]. A similar example involves bats, in
which species with greater WL forage in areas where there
are fewer obstacles to detect and avoid [49]. On the other
side, increased WL consistently decreased escape perform-
ance in a bird [50].
Despite higher WL requires higher wing-beat fre-
quency and increases flight cost [51], flight speed gener-
ally increases with WL [11,52], so that higher WL could
be positively selected in specific contexts. For example,
males of perching butterfly species (which sit and wait
on prominent landmarks and rapidly take off to inter-
cept females) had higher WL than patrolling closely-
related species [53]. AtM-species may thus fly faster
while sacrificing manoeuvrability (an important factor
while carrying loads) than UtM-species. These consider-
ations, together with the observed negative covariation
of FMR and WL across species, suggest that the selection
pressures related to foraging (load-lifting/manoeuvrability)
constitute the main determinants of flight morphology in
central-place foraging Hymenoptera.
Moreover, among AtM species, investment in flight
muscles and wing size, which would be of limited adap-
tive value during foraging, may further be counteracted
by contrasting selection acting on other life-history
traits, such as reproductive investment. In butterflies, for
example, palatable species have higher FMR because of
higher predation risk and stronger escape demands, but
also smaller ovaries than unpalatable species, suggesting
that investment in the flight apparatus and predator
avoidance trades off with investment in reproduction
[2]. Intriguingly, a preliminary analysis based on litera-
ture data suggests that this could be the case also among
the Apoidea. In fact, the number of ovarioles per ovary
was significantly higher in bees (3.6 ± 0.09, n = 32 spe-
cies) than in apoid wasps (2.9 ± 0.03, n = 75 species)
(t
39
= 6.8, P < 0.0001) (data from [54,55]; highly eusocial
bee species (queens), parasitoid apoid wasps and brood-
parasitic apoid wasps were not considered because of
their peculiar life-style). Though it might be speculated
that eusocial bee species represent an exception to this
pattern, we note that honeybee workers can have from 1
to 12 ovarioles per ovary (with an average of about 4)
[56], thus roughly agreeing with the rest of bees. In
addition, workers of one species of Bombus (the primi-
tively eusocial B.morio) have the same number of ovari-
oles per ovary as related solitary species (4) [54]. This
hypothesis, however, needs a robust, phylogenetically con-
trolled, test, using species for which both flight morph-
ology and measurements of fecundity are available.
Conclusion
Our findings suggest that load-carrying constraints re-
lated to foraging have affected the evolution of flight
morphology in flying central-place foraging Hymenop-
tera, and that release from these constraints, which took
place with the evolution of food load manipulation abil-
ity, has selected against the maintenance of a costly
flight apparatus, which could possibly be traded against
reproductive investment.
Materials and methods
Sample collection and morphological measurements
We collected data on species from the two superfamilies
Apoidea (families Apidae, Crabronidae, Megachilidae,
Sphecidae) and Vespoidea (family Vespidae), including
bees (pollen/nectar collectors) and wasps (prey collec-
tors) (Table 1). A total of 216 females from 21 species
[5–35 females per species, 10.8 ± 7.2 (s.d.) females per
species on average] were caught in the field, in natural
populations found in the Parque Natural de la Albufera,
Valencia province (South-Eastern Spain), during the
spring-summer 2009–2010. Specimens were determined
to species level following taxonomic keys [57-59] and
with the aid of experts; however, for seven of them we
could only reach the genus level and therefore assigned
specimens to morphospecies (Table 1). Additional data
for seven species were obtained from the literature
(Table 1). Overall, 14 species fell in the AtM group and
14 species in the UtM group. Bees and wasps were killed
by freezing upon collection. Within 2–3 hours, females
were weighed in the lab with an electronic balance (to
the nearest 0.002 g) (M
b
, body mass). We then separated
the thorax from the rest of the body and weighed it
(M
t
, thorax mass). FMR was calculated as (0.95 × M
t
/M
b
)
for individual specimens [6], and the average value within
species was used in interspecific comparisons. For each
species, we further calculated the predicted maximum
food load mass which can be carried in flight after a suc-
cessful take-off (Load
max
) according to the regression
equation of maximum lift force vs. flight muscle mass for
bees and wasps provided in Table five of [6]. Finally, by
adding M
b
to Load
max
, we calculated the total maximum
load mass which can be carried (M
max
).
Polidori et al. Frontiers in Zoology 2013, 10:36 Page 7 of 11
http://www.frontiersinzoology.com/content/10/1/36
One wing pair (forewing and hindwing) was gently
separated from the thorax, and then scanned on an
Epson 2450 flatbed scanner (720 dpi). NIH ImageJ was
used to determine individual wing area; total wing area
(A
w
) refers to the area of both wing pairs and was
obtained by doubling the previous measurements. We
then calculated the wing loading WL (M
b
/A
w
) [10] for
each individual, and the average value within species was
used in interspecific comparisons. Measures were taken
to the nearest 0.002 mm.
As wet body mass can be confounded by body condi-
tion and water content, we repeated the calculations of
FMR and WL using dry mass (after oven-drying all body
parts for 48 hours at 70 °C). In addition, we also mea-
sured the head width (a good predictor of body size in
Hymenoptera, e.g. [60]) with a digital calliper (to the
nearest 0.02 mm) to obtain a condition-independent
body size estimate (Additional file 1: Table S2). For the
sample of species we collected, the correlation between
wet and dry mass was very high (r = 0.89, n = 21 species,
log
10
-transformed variables). Moreover, there was a strict
positive correlation between head width and wet mass
(r = 0.90, n = 21 species, log
10
-transformed variables).
Therefore, in the following analysis we used wet mass
instead of dry mass because dry mass was not available
for the seven species for which we obtained data from
the literature (Table 1). Using wet mass instead of dry
mass did not affect our conclusions (see also Results), as
wet body mass truly reflects across-species differences in
body size. Importantly, it is the wet mass that needs to be
lifted by the insects and therefore it is the most relevant
variable to measure from an eco-evolutionary standpoint.
For the morphological variables we recorded (M
b
,M
t
,
A
w
), the variance among species was significantly larger
than the variance within species (F-values always > 18,
P < 0.0001).
Molecular analyses
In comparative studies, species cannot be considered as
independent sampling units as their shared ancestry may
affect actual phenotypic values [61,62]. For this reason,
we built a molecular phylogeny of the studied species to
conduct comparative analyses accounting for phylogen-
etic relationships among species.
Tissue samples of the measured individuals could not
be stored in suitable conditions to allow for genetic ana-
lyses; we therefore used sequences of a fragment of the
18S rRNA gene and of the 28S rRNA gene of 28 selected
taxa of Apoidea and Vespoidea retrieved from GenBank.
Whenever possible, we retrieved sequences from the
same species for which we had morphological data; if no
sequences were available for a given species, sequences
from congeneric species were used. The complete list of
taxa and GenBank accession numbers is provided in
Additional file 1: Table S1. Homologous 18s rRNA and
28s rRNA gene sequences of Scolebythus madecassus
(Evans) (Hymenoptera: Chrysidoidea) were used as an
outgroup.
Sequences were aligned using CodonCode Aligner
(v. 3.7.1.1, Codon Code Corporation). GBlocks [63] was
used to delete highly divergent regions which could either
not be unambiguously aligned or were saturated by mul-
tiple substitutions, or required assumption of multiple
indels.
Preliminary analyses showed congruencies both in
terms of topology and support between Bayesian and
Maximum Likelihood phylogenetic analyses; we there-
fore decided to perform the analyses of this study using
the faster Bayesian algorithm. Partitioned Bayesian infer-
ence searches were performed using MrBayes 3.1.2 [64]
with the following 2 partitions: 18S rRNA gene and 28S
rRNA gene. The best-fitting model of substitution for each
partition was determined by AIC in jModeltest [65] and
the GTR + I + G model was selected for both partitions.
To obtain a topology congruent with the most recent
and well-established phylogenetic hypotheses, the follow-
ing three constraints were used in the Bayesian phylogen-
etic analyses: (a) Sphecidae were constrained in basal
position to the Crabronidae, Apidae and Megachilidae; (b)
Crabronidae were constrained as monophyletic; (c) Apidae
and Megachilidae were constrained as monophyletic [66].
We performed two runs of 10 million generations
(started on random trees) and four incrementally heated
Markov chains (using default heating values) each, sam-
pling the Markov chains at intervals of 1000 generations.
Stabilization and convergence of likelihood values was
checked by visualizing the log likelihoods associated with
the posterior distribution of trees in the program Tracer
[67]. The first five million generations were conserva-
tively discarded and five millions trees were retained
post burn-in and summed to generate the majority rule
consensus tree (Figure 1).
Likelihood unequivocal reconstruction of character
evolution was performed using the ancestral state mod-
ule implemented in MESQUITE (Version 2.75; [68]).
The character evolution and ancestral states were
reconstructed by mapping the character “food manipula-
tion ability”(as a binary categorical trait, UtM vs. AtM)
on the rooted topology generated from the previously
described MrBayes analyses (Figure 1). As a major ad-
vantage, Maximum Likelihood takes branch lengths into
account and allows quantifying the uncertainty associ-
ated with each reconstructed ancestral state [69]. For the
likelihood apomorphic trends and ancestral state recon-
struction we used the symmetrical Markov k-state one-
parameter model (MK1) [70], which assumes a single
rate of transition between two character states, and any
particular change is equally probable. The likelihoods
Polidori et al. Frontiers in Zoology 2013, 10:36 Page 8 of 11
http://www.frontiersinzoology.com/content/10/1/36
are reported as proportional likelihoods and are indi-
cated as pie charts in Figure 1. Likelihood ratios at a
node are compared by pairs, and the conventional cut-
off point for assessing the significance of one state at a
given node over the other (defined as a ‘rule-of-thumb’
[69]) is if their likelihoods differ by more than 2 log
units (default setting in Mesquite).
Statistical analyses
The relationships between flight morphology (FMR and
WL) and food load manipulation ability (UtM vs. AtM)
were analysed while accounting for common ancestry ef-
fects in the data (Felsenstein 1985; Garland et al. 1992).
We controlled for phylogeny by means of phylogenetic
generalized least-squares (PGLS) models [71-73], as
implemented by the ‘ape’library [74] of the software R
(version 2.8.1) (R Development Core Team 2008). The
phylogenetic variance–covariance matrix was obtained
by the ‘corPagel’function. The level of phylogenetic
autocorrelation of species’traits included in a PGLS
model was expressed in terms of the λindex [72], that
varies between 0 (phylogenetic independence) and 1
(species’traits covary in proportion to their shared evo-
lutionary history). PGLS models including the phylogen-
etic variance-covariance matrix multiplied by λreturn
phylogenetically corrected parameter estimates of co-
variation between phenotypic traits [72,73]. We tested
whether the degree of phylogenetic dependence among
traits was statistically significant by comparing a model
where λwas set to 0 (i.e. assuming phylogenetic independ-
ence) with the model where it was allowed to reach its
maximum likelihood value, according to a Brownian mo-
tion model of character evolution [74], by means of likeli-
hood ratio (LR) tests [73]. We built two PGLS models,
testing whether food load manipulation ability (0 = UtM;
1 = AtM) affected FMR and WL, respectively. In all
models, we included body mass (log
10
-transformed) as an
additional covariate. This was especially relevant for the
model of WL, since this variable is known to scale
allometrically with body mass across insect species
according to a power function [51,75], and this was the
case also in the present dataset (exponent of the power
function = 0.394, F
1,22
= 45.9, P < 0.001, r
2
= 0.68). To
linearize the relationship between WL and body mass, we
therefore log
10
-transformed both variables before includ-
ing them in all statistical models. Model residuals were
normally distributed in all cases (Lilliefors test, P-values
always > 0.16). Visual inspection of the data suggested that
the variances in WL might differ according to food load
manipulation (see Figure 2b). However, accounting for
heterogeneity of variances in the PGLS model, by allowing
the two levels of the covariate of food load manipulation
to have different variances (see [76] for details), did not
significantly improve model fit (LR test, P = 0.59), and did
not qualitatively alter our conclusions (details not shown
for brevity). We therefore report estimates from models
not controlling for heteroscedasticity.
Finally, we analysed the covariation between FMR and
WL by running a PGLS with WL as the dependent vari-
able and FMR and body mass as predictors. Parameter
estimates and mean values are reported together with
their associated standard error (s.e.).
Additional file
Additional file 1: Table S1. List of taxa and GenBank accession numbers
of sequences used in the phylogenetic reconstruction. Table S2. Thorax
mass (M
t
), maximum food load that females could theoretically carry in
flight after a successful take-off (Load
max
), maximum total load that females
could theoretically carry in flight (M
max
= body mass + Load
max
), maximum
% of food load that females could theoretically carry relative to body mass
((Load
max
/body mass) × 100)), total area of the wings (A
w
) and head width
(HW) for the species used in the study. Category of food manipulation
ability is reported (0 = unable to manipulate food load, 1 = able to
manipulate food load). Table S3. PGLS models testing the effects of food
load manipulation ability (0 = UtM; 1 = AtM) on flight muscle ratio (FMR) and
(log
10
-transformed) wing-loading (WL) calculated based on dry body mass
values, while controlling for head width (log
10
-transformed) as an index of
body size (n= 21 species). The maximum likelihood estimate value of λ,
assessing the degree of phylogenetic dependence among the tested
variables (see Materials and methods), is shown for each model.
Abbreviations
FMR: Flight muscle ratio; WL: Wing loading; AtM: Able to manipulate food
load; UtM: Unable to manipulate food load; M
b
: Body mass; M
t
: Thorax mass;
Load
max
: Maximum food load that females could theoretically carry in flight
after a successful take-off; M
max
: Maximum total load (Load
max
+M
b
) that
females could theoretically carry in flight after a successful take-off; A
w
: Total
area of the wings; HW: Head width.
Competing interests
The authors have declared that no competing interests exist.
Authors’contributions
CP designed the study. CP, LD and JS sampled the species in the field. CP
and LD collected the morphological data. AC performed the phylogenetic
reconstruction. DR, CP and NS carried out the statistical analyses. CP, DR and
AC drafted the manuscript. All the authors read and approved the final
manuscript.
Acknowledgements
Thanks are due to Josè Tormos, who helped with species identification. Pau
Mendiola helped with sample collection. Davide Santoro and Heike Feldhaar
kindly provided pictures for Figure 1. CP’s research was supported by a JAE-
Doc post-doctoral contract (funded by the Spanish Research Council (CSIC)
and the FSE) and by the program “Estades temporals per a Investigadors
Convidats”of the University of Valencia (Spain). The work of AC was
supported by a postdoctoral grant from the Fundação para a Ciência e a
Tecnologia (FCT) (SFRH/BPD/72908/2010). We acknowledge support of the
publication fee by the CSIC Open Access Publication Support Initiative
through its Unit of Information Resources for Research (URICI). Finally, we
thank J. H. Marden and an anonymous referee for constructive criticism on
an earlier version of the manuscript.
Author details
1
Departamento de Biodiversidad y Biología Evolutiva, Museo Nacional de
Ciencias Naturales (CSIC), C/ José Gutiérrez Abascal 2, 28006 Madrid, Spain.
2
CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos,
Campus Agrário de Vairão, Rua Padre Armando Quintas, Vairão, Vila do
Conde 4485-661, Portugal.
3
Department of Biology, McGill University, Stewart
Biology Building, Docteur Penfield 1205, Montreal, Quebec H3A 1B1, Canada.
Polidori et al. Frontiers in Zoology 2013, 10:36 Page 9 of 11
http://www.frontiersinzoology.com/content/10/1/36
4
Departament de Zoologia, Universitat de València, C/Dr. Moliner 50,
València, Burjassot 46100, Spain.
5
Dipartimento di Bioscienze, Università degli
Studi di Milano, Via Celoria 26, Milano 20133, Italy.
Received: 19 March 2013 Accepted: 20 June 2013
Published: 28 June 2013
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doi:10.1186/1742-9994-10-36
Cite this article as: Polidori et al.:Food load manipulation ability shapes
flight morphology in females of central-place foraging Hymenoptera.
Frontiers in Zoology 2013 10:36.
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