Season length, body size, and social polymorphism: size clines but not saw tooth clines in sweat bees: Season length, body size, and social polymorphism

Abstract

Annual insects are predicted to grow larger where the growing season is longer. However, transitions from one to two generations per year can occur when the season becomes sufficiently long, and are predicted to result in a sharp decrease in body size because available development time is halved. The potential for resulting saw-tooth clines has been investigated only in solitary taxa with free-living larvae. 2. Size clines were investigated in two socially polymorphic sweat bees (Halictidae): transitions between solitary and social nesting occur along gradients of increasing season length, characterised by the absence or presence of workers and offspring that are individually mass provisioned by adults. How the body size changes with season length was examined, and whether transitions in social phenotype generate saw-tooth size clines. We measured Lasioglossum calceatum and Halictus rubicundus nest foundresses originating from more than 1000 km of latitude, encompassing the transition between social and solitary nesting. 3. Using satellite-collected temperature data to estimate season length, it was shown that both species were largest where the season was longest. Body size increased linearly with season length in L. calceatum and non-linearly in H. rubicundus but the existence of saw-tooth clines was not supported. 4. The present results suggest that because the amount of food consumed by offspring during development is determined by adults, environmental and social influences on the provisioning strategies of adult bees may be more important factors than available feeding time in determining offspring body size in socially polymorphic sweat bees.

Full text

Ecological Entomology (2017), DOI: 10.1111/een.12448
Season length, body size, and social polymorphism:
size clines but not saw tooth clines in sweat bees
PAUL J. DAVISON
∗and JEREMY FIELD
∗School of Life Sciences, University of Sussex,
Brighton, U.K.
Abstract. 1. Annual insects are predicted to grow larger where the growing season is
longer. However, transitions from one to two generations per year can occur when the
season becomes sufciently long, and are predicted to result in a sharp decrease in body
size because available development time is halved. The potential for resulting saw-tooth
clines has been investigated only in solitary taxa with free-living larvae.
2. Size clines were investigated in two socially polymorphic sweat bees (Halictidae):
transitions between solitary and social nesting occur along gradients of increasing season
length, characterised by the absence or presence of workers and offspring that are
individually mass provisioned by adults. How the body size changes with season length
was examined, and whether transitions in social phenotype generate saw-tooth size
clines. We measured Lasioglossum calceatum and Halictus rubicundus nest foundresses
originating from more than 1000 km of latitude, encompassing the transition between
social and solitary nesting.
3. Using satellite-collected temperature data to estimate season length, it was shown
that both species were largest where the season was longest. Body size increased linearly
with season length in L. calceatum and non-linearly in H. rubicundus but the existence
of saw-tooth clines was not supported.
4. The present results suggest that because the amount of food consumed by offspring
during development is determined by adults, environmental and social inuences on
the provisioning strategies of adult bees may be more important factors than available
feeding time in determining offspring body size in socially polymorphic sweat bees.
Key words. Body size, eusociality, size cline, social polymorphism, sweat bee.
Introduction
Intraspecic geographic variation in life history traits is common
in many taxa (Roff, 1992; Stearns, 1992), and spatial variation in
body size has received considerable research attention for more
than 150 years (Blanckenhorn & Demont, 2004). In insects,
body size can have a key inuence on traits such as potential
fecundity, resources allocated to offspring, thermoregulation,
and overwintering success (May, 1979; Honˇ
ek, 1993; Fox &
Czesak, 2000; Hunt & Simmons, 2000; Smith, 2002; O’Neill
et al., 2014). Within species, body size frequently varies either
positively or negatively with latitude and altitude (Chown &
Gaston, 2010; Shelomi, 2011). Positive relationships are known
Correspondence: Paul J. Davison, College of Life and Environ-
mental Sciences, Centre for Ecology and Conservation, University
of Exeter, Penryn Campus, Cornwall, TR10 9EZ, U.K. E-mail:
p.davison89@gmail.com
∗Current address: College of Life and Environmental Sciences, Centre
for Ecology and Conservation, University of Exeter, Penryn Campus,
Cornwall, TR10 9EZ.
as Bergmann clines (BCs) (Bergmann, 1847; Ray, 1960, but see
Wat t et al., 2010), negative ones as converse-Bergmann clines
(CBCs) (Park, 1949; Blanckenhorn & Demont, 2004).
In seasonal environments, insects can grow and reproduce
only during the active season (Bradshaw & Holzapfel, 2007;
Gullan & Cranston, 2010), which becomes progressively shorter
with increasing latitude and altitude (Bradshaw & Holzapfel,
2007). Annual insects with long generation times can exhibit
CBCs if a larger body size can be attained only by pro-
longing growth (Chown & Gaston, 1999; Blanckenhorn &
Demont, 2004). Correspondingly, CBCs are observed in insects
such as butteries and crickets (e.g. Nylin & Svärd, 1991;
Mousseau, 1997), and are frequently found to have a genetic
basis (Masaki, 1967; Blanckenhorn & Fairbairn, 1995; Telfer
& Hassall, 1999). In contrast, species with many generations
per year in which growth is not limited by season length can
exhibit BCs, either because it is adaptive or as a consequence
of temperature-mediated physiological processes (see Blanck-
enhorn & Demont, 2004 and references therein).
© 2017 The Authors. Ecological Entomology published by John Wiley & Sons Ltd on behalf of Royal Entomological Society 1
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any
medium, provided the original work is properly cited.

2Paul J. Davison and Jeremy Field
Season length
Development time
and body size
Transition zone
Univoltine Bivoltine
Fig. 1. A hypothetical saw-tooth cline, after Roff (1980) and Nygren
et al. (2008). In socially polymorphic sweat bees, univoltine populations
are solitary while bivoltine populations are social.
When the season becomes sufciently long, tness can be
maximised by adopting a bivoltine life cycle (Masaki, 1972;
Roff, 1980), because any benets of reaching a larger size
are offset by increased mortality risk during development (e.g.
Johansson & Stoks, 2005). As the time available for each
generation to develop is halved at the transition from univoltine
to bivoltine life cycles, Roff (1980) predicted that there should
be a concomitant sharp drop in body size (Fig. 1). As predicted,
saw-tooth size clines are observed in a variety of groups where
there are latitudinal changes from univoltine to bivoltine life
cycles, including crickets (Masaki, 1972; Mousseau & Roff,
1989), butteries (Nygren et al., 2008), and moths (Välimäki
et al., 2013). However, saw-tooth size clines are not always
found and the relationships between body size and season
length may be complex (Kivelä et al., 2011; Välimäki et al.,
2013). For example, counter gradient variation occurs where
a higher growth rate evolves to counter the effect of a shorter
available development time, which can over, under, or perfectly
compensate for clinal variation in development time (Conover
& Schultz, 1995; Blanckenhorn & Demont, 2004).
Socially polymorphic sweat bees (Hymenoptera: Halictidae)
are a group in which the presence of saw-tooth clines might
have more far-reaching implications. The same species can
exhibit both solitary and social behaviour, characterised by
either the absence or presence of a rst brood of workers
before the production of reproductives (Fig. 2; Schwarz et al.,
2007). Each spring, mated females (foundresses) emerge from
hibernation and initiate subterranean nests. Foundresses then
mass provision a series of separate brood cells with a ball of
pollen and nectar, providing each offspring with all the food
required for development. In solitary nests, all female offspring
mate and enter directly into hibernation. In social nests, however,
B1 females are typically smaller than the foundress (Packer &
Knerer, 1985; Schwarz et al., 2007), and at least some remain
at the nest as workers to help rear a second brood (B2) of
reproductive offspring.
Whether social or solitary behaviour is expressed correlates
closely with season length, and is analogous to the univoltine
and bivoltine populations of solitary taxa such as butteries,
moths, and crickets. Bees can nest socially only in southern or
Fig. 2. Being social takes longer than nesting solitarily. Brood rearing
in the solitary life cycle is completed when offspring provisioned by the
foundress emerge, but in the social life cycle offspring must provision a
second brood as workers. In both cases the life cycle must be completed
before the end of the season.
lowland areas where the season is sufciently long to rear two
consecutive broods (Fig. 2; Soucy & Danforth, 2002; Davison &
Field, 2016). Previous studies have generally found that sweat
bees in more northern or upland areas are smaller and follow
CBCs (Richards & Packer, 1996; Soucy, 2002; Field et al., 2012;
Davison & Field, 2016, but see Sakagami & Munakata, 1972),
although measurements have been made only at widely scattered
sites hundreds of kilometres apart. Field et al. (2012) predicted
that socially polymorphic sweat bees could exhibit saw-tooth
size clines, because double-brooded bees just to the south of the
transition might be more time stressed than single-brooded bees
just to the north (Fig. 1). Body size is strongly correlated with
the amount and quality of food consumed during development
(Plateaux-Quénu, 1983; Richards & Packer, 1994; Roulston &
Cane, 2002). Thus, offspring size might also be inuenced by
environmental constraints on, and strategic investment decisions
by, adult bees at the time of provisioning (Richards & Packer,
1996; Field et al., 2012; Richards et al., 2015).
In the present study, how transitions in social phenotype can
impact on the body size of foundresses is examined. The pres-
ence is tested for of saw-tooth clines in two socially polymorphic
sweat bees along a gradient of increasing season length, from
the north of the United Kingdom (UK) southwards to western
France. Lasioglossum calceatum Scopoli and Halictus rubicun-
dus Christ are widely distributed throughout the Palaearctic and
Holarctic, respectively, (Pesenko et al., 2000; Pesenko, 2005),
and each is socially polymorphic throughout its range (Sakagami
& Munakata, 1972; Soucy & Danforth, 2002; Field et al., 2010,
2012; Davison & Field, 2016). In the UK, both species nest
socially in southern or lowland areas, but solitarily in northern
and upland environments (Field, 1996; Soro et al., 2010; Field
et al., 2012; Davison & Field, 2016). The present results gener-
ally support the existence of CBCs in both species, but not the
existence of saw-tooth clines.
Materials and methods
Sampling range
Although L. calceatum is known to nest socially in west-
ern France (Plateaux-Quénu, 1992), no studies on the social
behaviour of H. rubicundus from France have been published.
© 2017 The Authors. Ecological Entomology published by John Wiley & Sons Ltd on behalf of Royal Entomological Society
Ecological Entomology, doi: 10.1111/een.12448

Season length, body size, and social polymorphism 3
Lasioglossum
calceatum
Halictus
rubicundus
(a) (b)
Fig. 3. Maps showing the locations from which specimens were collected within the United Kingdom and France for specimens of (a) Lasioglossum
calceatum and (b) Halictus rubicundus that were measured and entered into the size cline analysis. Note that the number of specimens sampled from
each location is not indicated.
However, it is highly likely that H. rubicundus nests socially in
the regions of France sampled in this study. Halictus rubicundus
nests socially in southern Britain (Soro et al., 2010; Field et al.,
2012), and elsewhere in its range, the expression of social pheno-
type is closely linked to latitude and altitude (Soucy & Danforth,
2002). Therefore, although at present it is not known exactly
where the transition from solitary to social occurs, the range of
latitudes sampled for both species is expected to encompass the
transition zone.
Specimens
Specimens were sourced from museum, private, and university
collections spanning the years 1895–2014. In total, 487 L.
calceatum and 356 H. rubicundus specimens from Britain and
France were measured, covering 45– 58 and 47 – 58 degrees
of latitude, respectively (Fig. 3). Bee size was recorded as
foundress head width (HW), measured at the widest point of
the head in full-face view including the compound eyes. HW
is a widely used proxy for body size in sweat bees (e.g. Soucy,
2002; Brand & Chapuisat, 2012), which correlates strongly with
overall size and mass (Michener & Lange, 1958; Stubbleeld &
Seger, 1994; Potts, 1995; Roulston & Cane, 2000) and does not
change after death (Daly, 1985). HW is advantageous because
the head capsule also does not degrade with age, whereas the
wings of older bees can become frayed and difcult to measure.
In the present study, we focus on nest foundresses only.
Lasioglossum calceatum and H. rubicundus workers are typi-
cally smaller than foundresses (Field et al., 2012; Davison &
Field, 2016; but see Field et al., 2010), therefore to ensure work-
ers did not confound the analysis we excluded bees caught after
15 June. This cut-off is justied because in southern UK (where
season length is longest in the UK) L. calceatum B1 offspring
have never been observed before July (Davison & Field, 2016),
and the earliest H. rubicundus B1 offspring have been observed
only in the second half of June (Field et al., 2010, 2012). Further
south in France, L. calceatum workers are typically observed
earlier; however, all French specimens of both species were cap-
tured in either March or April, well before the period of worker
emergence (Plateaux-Quénu et al., 2000).
The location and date of capture were recorded for all spec-
imens. Data on specimen labels varied considerably in detail
from precise geographic coordinates and date of capture to
vague or indecipherable place names without a date. Specimens
without a veriable location or date of capture were excluded. If
the only location data were a veriable place name (i.e. a town)
this was considered sufciently accurate, and coordinates for the
town were used as the given location for the specimen. Coordi-
nates were obtained from Google Maps©. Many specimen labels
© 2017 The Authors. Ecological Entomology published by John Wiley & Sons Ltd on behalf of Royal Entomological Society
Ecological Entomology, doi: 10.1111/een.12448

4Paul J. Davison and Jeremy Field
provided an Ordnance Survey (OS) grid reference, the national
coordinate system used in Great Britain. Locations given by
OS coordinates were determined using the Grab a Grid Refer-
ence Tool provided by the Bedfordshire Natural History Soci-
ety (available at http://www.bnhs.co.uk/focuson/grabagridref/
html/). The tool shows a satellite image map and a square over-
laying the area referred to by the given OS coordinate, which
varied from two to three gures in accuracy. In each case, the
centroid of the square was taken as the specimen location and
its coordinates obtained from Google Maps©. Depending on
the accuracy of the OS coordinates given, squares were either
100 ×100 m or 1 ×1 km.
HW measurements of most specimens were made at the
University of Sussex using a Leica binocular stereomicroscope
with an eyepiece graticule. Specimens kindly made available
by the Oxford University Museum of Natural History were
measured digitally on site. Twenty sweat bees to measure twice
were selected, and obtained a measurement error of 0.8%.
Estimating season length
Season length at all sampling locations was estimated as a
measure of the time available in the year for growth and repro-
duction. The number of days on which land surface temper-
ature (LST) exceeds 16 ∘Cinanaverageyearwasusedto
estimate the likely length of the active bee season (Kocher
et al., 2014). To estimate season length, emporal Fourier pro-
cessed LST data were used from the National Oceanographic
and Atmospheric Administration’s (NOAA) Advanced Very
High-Resolution Radiometer (AVHRR) polar-orbiting satellites
(Hay et al., 2006). Temporal Fourier analysis is a noise reduction
technique that describes variation in naturally occurring cycles
such as temperature as a series of summed sine curves of dif-
ferent amplitude and phase (Rogers, 2000; Scharlemann et al.,
2008). Data are based on 14 daily images at a spatial resolution
of 8 ×8 km, spanning a 20-year time series from August 1981
to September 2001. The annual, bi-annual, and tri-annual cycles,
which together describe over 90% of variation from the origi-
nal data (Hay et al., 2006), were utilised to reconstruct average
annual LST proles for each sampling location.
Temporal Fourier processed data were imported into the
software ArcGIS (Version 9.3), where the amplitude, phase,
and mean LST for each 8 ×8 km grid cell containing sampling
locations were extracted using the ‘sample’ function. Averaged
annual LST proles for each grid cell (td) were reconstructed
by summing (eqn 1) the annual (eqn 2), bi-annual (eqn 3), and
tri-annual (eqn 4) sine curves and adding the mean LST
td =∑
i
ti+ao(1)
where i=1–3
t1=a∗
1sin (((d+365∕4−p1)∗2∗𝜋)∕365)(2)
t2=a∗
2sin (((d+182.5∕4−p2)∗2∗𝜋)∕182.5)(3)
t3=a∗
3sin (((d+121.66667∕4−p3)∗2∗𝜋)∕121.66667)
(4)
where tiis the given temperature prole, aiis the amplitude
and pithe phase of the annual, bi-annual and tri-annual cycles
receptively, dis days (1–365) in the year, and a0the mean LST.
Kocher et al. (2014) was followed by calculating season length
for each grid cell as the number of days from the averaged annual
LST prole (td) on which the LST was greater than 16 ∘C.
Statistical analysis
For the data to support the saw-tooth hypothesis, body size
should follow the non-linear pattern shown in Fig. 1. As it is
unknown precisely where transitions between social and soli-
tary behaviour occur, Kivelä et al. was followed (2011) and
used polynomial regression to test objectively whether latitudi-
nal size variation in L. calceatum and H. rubicundus supports the
saw-tooth hypothesis. Specimens collected in the same 8 ×8km
grid cell returned the same value for season length, and spec-
imens were caught in different years. For each species, we,
therefore, used a generalised linear mixed model (GLMM) to
analyse clinal variation in head width and included ‘grid cell’
and ‘year’ as random effects. Explanatory variables included
were season length, the square of season length, and the cube
of season length (Kivelä et al., 2011). Support for the saw-tooth
hypothesis would be indicated if the model generated a signi-
cant positive cubic term for season length. Maximal models were
checked for normality and heteroscedasticity of residuals before
proceeding with stepwise model reduction, beginning with the
highest order power terms (Crawley, 2013). In the analysis of H.
rubicundus, residuals were highly non-normal. Head width was,
therefore, transformed to the power of 5.45 before analysis, this
being selected as the optimal transformation using the function
powerTransform in the Rpackage ‘car’ (Fox & Weisberg, 2011).
Analyses were conducted in the Renvironment (R Core Team,
2013), using the lme4 package (Bates et al., 2015) for GLMMs.
Supporting data are available in Table S1.
Results
The head width for 487 L. calceatum and 313 H. rubicundus
foundresses (mean HW: L. calceatum =2.38 ±0.01 mm, H.
rubicundus =2.98 ±0.01 mm) was measured. The head width
increased signicantly with increasing season length in both
L. calceatum and H. rubicundus, supporting previous work
suggesting that sweat bees follow CBC. Neither species showed
evidence of following a saw-tooth cline (as in Fig. 1). However,
the precise relationship between head width and season length
differed between the two species (Table 1; Fig. 4a,b). In L.
calceatum, the head width increased linearly with season length,
following a classic CBC (Fig. 4a). In contrast, the head width in
H. rubicundus generated a signicant quadratic term for season
length, indicating that the relationship was not linear (Fig. 4b).
The head width in H. rubicundus appeared to show very little
response to season length until it began to increase at the longest
season lengths. Note that the regression lines shown in Fig. 4a,b
are derived from the model estimates, and thus take account of
‘year’ and ‘grid cell’ (i.e. the 8 ×8 km squares of given season
length) as random factors.
© 2017 The Authors. Ecological Entomology published by John Wiley & Sons Ltd on behalf of Royal Entomological Society
Ecological Entomology, doi: 10.1111/een.12448

Season length, body size, and social polymorphism 5
Tab l e 1 . Parameter estimates for linear mixed-effects models explaining variation in head width in relation to season length for Lasioglossum
calceatum and Halictus rubicundus.
Species Variable Estimate SE tP
L. calceatum Intercept 2.115 0.095 22.468
Season length 0.001 0.001 2.287 0.024*
Season length2−6.91 ×10−69.46 ×10−6−0.730 0.464
Season length33.10 ×10−73.53 ×10−71.131 0.311
H. rubicundus Intercept 39.716 9.542 4.162
Season length −0.918 0.315 −2.913 <0.001***
Season length20.003 0.315 3.167 0.002**
Season length3<0.001 <0.001 1.663 0.099
P-values were obtained by sequentially removing terms from the model. *P<0.05; **P<0.01; ***P<0.001.
Discussion
Previous studies of saw-tooth clines in body size have focused
exclusively on solitary taxa with free-living immature forms
(e.g. Mousseau & Roff, 1989; Kivelä et al., 2011). Socially
polymorphic sweat bees are mass provisioners and transition
from expressing solitary to social behaviour, characterised by
the presence or absence of a worker generation before the
production of reproductives (Soucy & Danforth, 2002). It
was found that while both L. calceatum and H. rubicundus
were largest where the season was longest, neither exhibited
saw-tooth clines of the kind hypothesised by Field et al. (2012)
and Davison and Field (2016).
Clinal variation in body size
Overall, the largest foundresses of both L. calceatum and
H. rubicundus were from areas where the season was longest,
supporting previous conclusions that sweat bees follow CBCs
(Richards & Packer, 1996; Soucy, 2002; Field et al., 2012; Davi-
son & Field, 2016). The body size in taxa with free-living imma-
ture forms such as butteries and crickets often follow CBCs,
supposedly because as season length gradually shortens further
north, immatures have less time to spend feeding and growing. In
sweat bees, however, mothers supply each developing offspring
with a single ball of pollen and nectar containing all the food it
will consume before reaching adulthood. As offspring body size
is highly correlated with the size and composition of the pro-
vision mass (Plateaux-Quénu, 1983; Richards & Packer, 1994;
Roulston & Cane, 2002), the variation in body size of offspring
is likely to primarily reect the provisioning strategies of adult
bees rather than the time available for offspring to feed per se.
Adult bees in more northern or upland populations may expe-
rience environments where resources are scarcer or available
for less time, or where frequently inclement weather means
there are fewer opportunities to provision and oviposit (Field,
1996; Richards, 2004; Field et al., 2012; Richards et al., 2015).
These effects probably increase the costs of provisioning (e.g.
Zurbuchen et al., 2010) and may lead northern foundresses to
allocate each offspring with less food relative to those further
south (Field et al., 2012, but see Kim & Thorpe, 2001). Indeed,
studies have shown that smaller offspring are produced in years
with poorer weather, and when fewer resources are available
(Richards & Packer, 1996; Richards, 2004).
When the season becomes sufciently long, populations of
socially polymorphic sweat bees can be social, with the nal
(B2) brood provisioned by workers. Workers may be able to
allocate more food to each offspring because as a group they
bring resources back to the nest more rapidly than does a
solitary foundress (Richards, 2004). Furthermore, as foraging
increases adult mortality (Kukuk et al., 1998; Cant & Field,
2001), and adult survival can signicantly decrease brood
mortality (Eickwort et al., 1996; Soucy, 2002; Zobel & Paxton,
2007), selection is likely to favour foundress provisioning
strategies that maximise both offspring size and foundress
survival (e.g. Jørgensen et al., 2011). In social nests, however,
the death of a single worker has less effect on the survival of
brood because other adults can still defend the nest (e.g. Smith
et al., 2003). Therefore, foundresses in solitary populations may
provision less intensively than workers in social nests (Field,
1996; Richards, 2004; Neff, 2008). In addition, more southern
social nests might contain more workers because foundresses
emerge earlier (Plateaux-Quénu, 1992; but see Richards et al.,
2015), more B1 females choose to work rather than enter hiber-
nation (e.g. Yanega, 1993) or there are additional worker broods
(Yanega, 1993; Strohm & Bordon-Hauser, 2003). As sweat bee
eggs are relatively large (Iwata & Sakagami, 1966), workers
in larger nests might collect resources faster than foundresses
can oviposit. If foundresses can nevertheless prevent workers
from laying their own eggs, female reproductive offspring
could be allocated with more resources (Frank & Crespi, 1989;
Boomsma & Eickwort, 1993), providing a further boost to the
body size of foundresses further south.
Countergradient variation in the growth rate could potentially
mitigate seasonal constraints on development time if bees evolve
faster growth rates where the season is shorter (Conover &
Schultz, 1995; Kivelä et al., 2011). However, eld transplants
of both H. rubicundus and L. calceatum have found no evidence
for genetic differences in development time between northern
and southern bees (Field et al., 2012; P. J. Davison and J. Field,
in prep.). Instead, growth rates in sweat bees appear to be plastic
and most heavily inuenced by temperature (Kamm, 1974;
Weissel et al., 2006; Field et al., 2012).
Difference between the two study species
Head width increased linearly with season length in L. cal-
ceatum but non-linearly in H. rubicundus, which showed almost
© 2017 The Authors. Ecological Entomology published by John Wiley & Sons Ltd on behalf of Royal Entomological Society
Ecological Entomology, doi: 10.1111/een.12448

6Paul J. Davison and Jeremy Field
120 140 160 180 200 220 240
1.6
1.8
2.0
2.2
2.4
2.6
2.8
Head width (mm)
UK
France
(a)
140 150 160 170 180 190
0
10
20
30
40
Season length (days)
Transformed head width*
UK
France
(b)
Fig. 4. Head width in relation to season length in (a) Lasioglossum
calceatum and (b) Halictus rubicundus. Note the difference in the
length of the x-axes. Lines shown are regression lines derived from
the model estimates (see Table 1). Open circles represent specimens
from the United Kingdom, crosses specimens from France. *Head
width for H. rubicundus is transformed to the power of 5.45 using the
powerTransform function in the R package ‘car’ (see Methods).
no change within the UK (Fig. 4). This contrasts with previous
studies of H. rubicundus in which foundresses in cooler or
more northern areas were smaller (Potts, 1995; Field et al.,
2012), suggesting that different results can be obtained when
focusing on only a small number of sites. The near-absence of
asizeclineinUKH. rubicundus in the present study suggests
that foundresses can maintain a consistent body size, perhaps
by concentrating the same investment into fewer offspring as
the season length shortens (e.g. Smith & Fretwell, 1974). This
effect is likely to be seen most clearly where bees are solitary
and offspring body size is determined by a lone foundresses. As
sweat bee foundresses are thought to provision only a single egg
per day (Richards, 2004), differences in the effect of tempera-
ture on daily activity levels could explain this pattern (Weiner
et al., 2011). For example, H. rubicundus is a larger bee than L.
calceatum (see Results), which might afford thermoregulatory
advantages and enable foundresses to y for longer on any
given day relative to L. calceatum (Stone, 1994; Bishop & Arm-
bruster, 1999, but see Field et al., 2012). However, there are no
data regarding how brood sizes might vary with the change of
season length in L. calceatum or H. rubicundus, and it would
be particularly fruitful to determine brood sizes of both species
across the range of latitudes within the UK studied in the present
paper.
Why not saw-tooth clines?
In some solitary taxa such as butteries and crickets, con-
straints on development may become apparent only in the
directly developing rst generation (Kivelä et al., 2011). This is
because directly developing offspring must complete their entire
life cycle, whereas the diapausing generation need only reach the
overwintering stage before completing development the follow-
ing spring (Kivelä et al., 2011). Consequently, saw-tooth clines
can be more pronounced when only the directly developing rst
generation from bivoltine populations is considered (Masaki,
1972; Nygren et al., 2008; Kivelä et al., 2011). The present
study focuses exclusively on the size of B2 offspring from social
nests, and it is possible that a saw-tooth cline might be detected
if we instead examined only B1 offspring from social nests. In
sweat bees, B1 workers must emerge sufciently early in the sea-
son to help rear a B2 (Hirata & Higashi, 2008; Field et al., 2010).
Moreover, smaller B1 offspring with a shorter period of growth
might allow more time in the season to produce larger B2 off-
spring, which probably increases adult B2 female overwintering
success (Sakagami et al., 1984; Beekman et al., 1998; Brand &
Chapuisat, 2012, but see Weissel et al., 2012).
As in most social insects, body size in socially polymorphic
sweat bees size is intrinsically linked to social phenotype
(Packer & Knerer, 1985; Schwarz et al., 2007, but see Field
et al., 2010). Sweat bee workers are typically smaller than nest
foundresses, and the production of smaller workers in sweat bees
is typically viewed as a form of maternal manipulation (Richards
& Packer, 1994; Brand & Chapuisat, 2012). Moreover, because
foundresses in social populations can lay eggs in both broods,
they have a potentially high residual reproductive value even
after provisioning their B1 offspring (Kindsvater & Otto, 2014).
By producing smaller B1 offspring, foundresses might conserve
resources and increase their chance of remaining alive to lay B2
eggs (Field et al., 2010, 2012).
Patterns analogous to caste-size dimorphism have also been
detected in solitary bivoltine sweat bees, in which rst gener-
ation offspring are smaller than second generation offspring
despite the absence of castes (Plateaux-Quénu et al., 1989, see
also Kim & Thorpe, 2001). This suggests that disparity in the
size of adults from spring and summer broods could occur inde-
pendently of sociality (Lin & Michener, 1972; Michener, 1990).
For example, resource availability may change during the year
(e.g. Kim & Thorpe, 2001), and rst-generation offspring may
not need to be as large because they typically do not have to
survive the winter. Investigating size clines in solitary bivoltine
sweat bees could, therefore, help to separate the relative impor-
tance of sociality and voltinism as factors inuencing how body
size responds to changes in season length.
© 2017 The Authors. Ecological Entomology published by John Wiley & Sons Ltd on behalf of Royal Entomological Society
Ecological Entomology, doi: 10.1111/een.12448

Season length, body size, and social polymorphism 7
Implications for sociality
Environmental constraints on foundress body size might also
generate clinal variation in caste-size dimorphism (Field et al.,
2012). This could have important implications for reproduc-
tive conict within nests, because foundresses may dominate
workers more easily when caste-size dimorphism is greater
(Kukuk & May, 1991; Richards & Packer, 1996, but see Field
et al., 2010). Field et al. (2012) proposed that foundresses
at higher latitudes might produce the smallest workers, to
maximise the time available for production of B2 offspring
that are sufciently large to endure hibernation in a harsher
climate. However, empirical data for L. calceatum and H. rubi-
cundus imply that caste-size dimorphism is actually greatest
in warmer areas (Sakagami & Munakata, 1972; Yanega, 1989;
Plateaux-Quénu, 1992; Soucy, 2002; Davison & Field, 2016),
a pattern mirrored in other social sweat bees (Packer et al.,
1989). It is not clear how these patterns are generated. In ants,
workers tend to be largest in cooler environments, possibly as
an adaptation against starvation (Heinze et al., 2003; Purcell
et al., 2016). In sweat bees, however, workers often live for
only a few days or weeks (P. J. Davison, pers. obs.). If there is
little advantage in maximising worker size (Strohm & Liebig,
2008), workers may not follow a size cline at all, and larger
southern foundresses might simply produce a larger number
of workers given more time and resources (e.g. Robin, 1988).
This would lead to a north– south cline of increasing caste-size
dimorphism due entirely to changes in foundress size (Frank &
Crespi, 1989). Further work simultaneously examining clines
in workers and queens could prove particularly fruitful, as well
as detailed studies of wild social nests to determine whether
nests situated further south nests contain a greater number of
workers.
Acknowledgements
We wish to thank the following institutions and people for the
loan of specimens included in the size cline analysis: Professor
Simon Potts and Rebecca Evans at the University of Reading;
the Natural History Museum of London, the World Museum
in Liverpool, Samantha Bailey, Mike Edwards, and Thomas
Wood. David Benz, University of Oxford provided access to the
AVHRR data, and Jörn Scharlemann kindly advised on analysis.
This work formed part of a studentship (1119965) awarded to
P.J.D. funded by the Natural Environment Research Council and
the University of Sussex, supervised by J.F.. We have no conict
of interest to declare.
Supporting Information
Additional Supporting Information may be found in the online
version of this article under the DOI reference:
10.1111/een.12448
Ta b l e S 1 . Head width, specimen capture location, and season
length data used in the study.
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Accepted 7 June 2017
Associate Editor: Hans Van Dyck
© 2017 The Authors. Ecological Entomology published by John Wiley & Sons Ltd on behalf of Royal Entomological Society
Ecological Entomology, doi: 10.1111/een.12448