ORI GIN AL PA PER

Reproductive allometry does not explainthe temperature-size rule in water striders(Aquarius remigis)

Jeff Arendt • Daphne Fairbairn

Received: 15 June 2011 / Accepted: 2 September 2011 / Published online: 10 September 2011� Springer Science+Business Media B.V. 2011

Abstract Most ectotherms follow the temperature-size rule meaning that individuals

growing up under cool conditions are larger as adults than those growing up in warm

conditions. This pattern is difficult to explain because growth is usually slower in the cold

meaning it takes longer to reach a larger adult size. One potential explanation for this

pattern is that the typical increase in fecundity with body size is steeper in cool envi-

ronments than it is in warm environments. As such, the relative gain in fecundity for being

larger in the cold would compensate for the extra time it takes to grow to that size. We

present the first empirical test of this model using the water strider Aquarius remigis.

Individuals were reared at either 20� or 25�C with subsampling at each instar to estimate

growth trajectories. At adult eclosion, half were switched to the alternate temperature and

all females isolated, mated, and reproductive output measured for 3 weeks. We found that

A. remigis does follow the temperature-size rule but that fecundity was highly plastic with

respect to laying temperature such that the slightly greater fecundity of those reared at

20�C was due to their larger size. Overall, those laying at 25�C were more fecund and

showed a positive relationship between body size and fecundity. Those laying at 20�C did

not show a significant relationship between size and fecundity. As such, the reproductive

allometry shows a pattern reverse to what would be needed for a larger size in the cold to

be adaptive in this species. Although A. remigis follows the temperature-size rule over this

temperature range, this is likely due to a constraint on growth and development rather than

being adaptive plasticity.

Keywords Body size � Temperature � Size-fecundity � Aquarius remigis

J. Arendt (&) � D. FairbairnDepartment of Biology, University of California at Riverside, Riverside, CA 92521-6000, USAe-mail: Jarendt@ucr.edu

D. Fairbairne-mail: Daphne.Fairbairn@ucr.edu

123

Evol Ecol (2012) 26:745–757DOI 10.1007/s10682-011-9524-4

Introduction

Body size correlates with most performance variables in ectotherms including both sur-

vival and reproductive output (Roff 1992; Stearns 1992; Sogard 1997; Hurst 2007). As

such, understanding why organisms vary in body size is necessary for developing a full

understanding of evolutionary patterns. One common size pattern found in ectotherms is

the ‘temperature-size rule’ in which animals growing at cooler temperatures mature at a

larger size than conspecifics growing at warmer temperatures (Atkinson 1994; Angilletta

2009). This pattern poses a significant challenge to life-history theory because it takes

longer to grow to a larger size in the cold and thus the likelihood of mortality prior to

reproduction is greater than in the warm (Berrigan and Charnov 1994). Several theoretical

models have been proposed to explain the temperature-size rule (reviewed in Angilletta

2009) including adaptive (Stearns and Koella 1986; Berrigan and Charnov 1994; Sibly and

Atkinson 1994; Arendt 2011) and non-adaptive (Van der Have and De Jong 1996; Ang-

illetta and Dunham 2003; Jarosik et al. 2004; Walters and Hassall 2006) explanations.

Despite the theoretical attention this problem has garnered, there have been few attempts to

test these models directly although Angilletta (2009) has collected data from the literature

to address several model assumptions.

Recently, Arendt (2011) suggested that reproductive allometry could explain the

temperature-size rule if fecundity increased more rapidly with size in cool environments

than in warm environments. Increased fecundity in the cold can thus compensate for the

added time needed to reach this size. The model describes the optimal size at maturation

for an organism with determinate growth (one that stops growing after maturation) pro-

vided one knows two relationships: (1) the growth trajectory (size at age), and (2) how

fecundity scales with size under different temperature regimes. Although environment-

dependent growth rates are well known (for reviews see Arendt 1997; Dmitriew 2011),

size-fecundity relationships are rarely measured under multiple conditions. This is likely

because organisms are usually assumed always to produce as many young as possible for a

given size so that the relationship should be constant for most conditions. However,

resource availability affects this relationship in a snake (Brown and Shine 2007) and

temperature affects it in Daphnia (Scheiner and Yampolsky 1998; Weetman and Atkinson

2004) and several insects (Carroll and Quiring 1993; Irwin and Lee 2000; Ellers et al.

2001; Berger et al. 2008). Although the size-fecundity relationship was not measured

directly, Drosophila melanogaster selected for different sizes show more of a difference in

fecundity when reared at cool temperatures than when reared at warm temperatures

(McCabe and Partridge 1997), a pattern consistent with the size-fecundity model. Only the

studies with Daphnia provided sufficient data to parameterize the model of Arendt (2011).

However, Cladocerans have indeterminate growth and thus are not an ideal test of the

model.

The present study tests the Arendt model using the water strider (A. remigis), an insect

with determinate growth and a pattern of phenotypic plasticity for body size (Fairbairn

2005) and development time (Blanckenhorn 1991a) that follows the temperature-size rule

(Fairbairn 2005). Water striders are true bugs (class Hemiptera) that inhabit streams and

small rivers across temperate North America (Preziosi and Fairbairn 1992; Fairbairn 2005).

Their common name derives from their habit of skating on the surface of the water where

they feed on the remains of insects carried on the current. Eggs are laid under the water

usually on rocks or on the stems of emergent vegetation. The nymphs climb to the water

surface on hatching and thereafter co-exist with adults on the stream surface. Under natural

conditions, daily, lifetime and instantaneous fecundity are strongly correlated with body

746 Evol Ecol (2012) 26:745–757

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size in female A. remigis primarily because of the direct relationship between number of

eggs and abdomen size (Fairbairn 1988a; Preziosi et al. 1996; Preziosi 1997; Preziosi and

Fairbairn 2000). Fecundity is also strongly influenced by food availability (Blanckenhorn

1991b; Blanckenhorn et al. 1995; Ferguson 2000) but its relationship to temperature

remains to be determined. Through most parts of its range, A. remigis lacks wings (i.e.,

they are apterous) and populations are restricted to dispersal along watercourses (Fairbairn

1986, 1988b). However, Californian populations consist of a mix of wingless and fully

winged (macropterous) adults and the latter readily disperse many kilometers between

streams (Kaitala and Dingle 1992; Fairbairn and King 2009). Because some individuals are

capable of dispersal, we expect both spatial and temporal heterogeneity in the temperature

experienced among individuals from a given natal site as well as across the life cycle of

any given dispersing individual.

Theory

The model of Arendt (2011) is adapted from that of Sibly and Atkinson (1994) and

depends upon two relationships. First is the relationship between size and age. Arendt

(2011) only developed models for linear growth but growth rates decrease with age in most

animals so we extend the model here. After comparing several linear and non-linear

regressions we found that growth in A. remigis was best described by a sigmoid rela-

tionship of the form

St ¼b

1þ e�ðt�t0Þ

k

ð1Þ

with St is size at time t, b is the asymptotic size, t0 describes the position of the curve on the

x axis, and k is the inverse of the growth constant for the curve. Next we need the

relationship between size and fecundity, in this case described as the straight line

n ¼ mSa þ c ð2Þ

with n is the number of offspring, m is the slope, Sa is adult size, and c is the intercept.

Substituting (Eq. 1) into (Eq. 2) yields

n ¼ cþ m b.

1þ e�ðtj�t0Þ=k� �� �

ð3Þ

with tj being the length of the juvenile period (i.e., age at maturation). Solving for tj yields:

tj ¼ t0 � k � lnmb� nþ c

n� c

� �: ð4Þ

Following Sibly and Atkinson (1994), the optimal age at maturation is then found by

maximizing the reproductive value at birth (V). Assuming spatial heterogeneity, this is

lifetime reproductive success discounted by e-Ft where F is the overall rate of increase of

an allele in the population and t is age (see Sibly and Curnow 1993). This is given by

V ¼ ne� ljþFð Þtj1� e� laþFð Þta

ð5Þ

Evol Ecol (2012) 26:745–757 747

123

where lj is juvenile mortality rate, la is adult mortality rate, and ta is age after maturation.

It turns out to be much simpler to analyze this equation if we substitute x = ln(n) for n.

Doing so and rearranging Eq. 5 yields

x� lj þ F� �

tj ¼ ln V 1� e� laþFð Þta� �h i

: ð6Þ

Note that this equation was incorrect in Arendt (2011). Maximum fitness if found by

differentiating age with respect to fecundity and setting to zero which yields dtj/dx = 1/

(lj ? F) (Sibly and Atkinson 1994). To get the optimal size at maturation, we first sub-

stitute n = ex into Eq. 4 then differentiate to get

dtj

dx¼ kex

mb� ex þ cð Þ ¼1

lj þ F� � ð7Þ

solving for ex yields

ex ¼ mbþ cð Þ1þ k lj þ F

� � : ð8Þ

Substituting this for n in Eq. 2 and rearranging yields an optimal size at maturation of

Sopt ¼mb� kc lj þ F

� �

mþ km lj þ F� � : ð9Þ

Because the growth rate of ectotherms is less in the cold (smaller k) than in the warm,

fecundity must scale more steeply with size (larger m) in order for the optimal size to be

greater. Under spatial heterogeneity the term lj ? F is assumed to be the same for both

temperatures but will be different under temporal heterogeneity (Sibly and Atkinson 1994).

As we shall see, the effect of this term is minor compared to the effect of fecundity.

Thus all we need do to test this model is measure the relationships given by Eqs. 1 and 2

on animals reared in two environments and enter the resulting parameters into Eq. 9. If a

larger size in the cold is adaptive for A. remigis, then Eq. 9 using values measured in the

cold should be greater than the value estimated when using values measured in a warm

environment, provided that both temperatures are within the ranges typically experienced

by the striders in the wild. Females that grew and reproduced under these two constant

temperature conditions were used to test the model. However, we also measured fecundity

on females that had been switched between temperatures following the adult molt. This

treatment allowed us to separate the direct effects of laying temperature on rate of egg

production from the effects of body size or other indirect effects of rearing temperature.

Hence it provides insight into the biological basis of the temperature-size relationship.

Methods

Adult A. remigis (119 females and 81 males) were collected from Rattlesnake Creek near

Santa Barbara, CA, USA on July 3, 2010 and transported to the University of California at

Riverside. Sexes were isolated into large holding tanks with circulating water and fed

frozen crickets (Acheta domesticus) and fruit flies (Drosophila melanogaster). Females

were provided with Styrofoam cups for the laying of eggs and fed ad libitum for 10 days to

minimize residual effects from the field. A. remigis are income breeders and lay eggs daily

748 Evol Ecol (2012) 26:745–757

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for several months under laboratory conditions. Previous experiments have demonstrated

that daily fecundity responds to altered food levels in less than 7 days (Ferguson 2000). In

our populations, females eclose without eggs and there is a lag of one to several weeks

before egg production begins. After 10 days, all cups were replaced so that eggs used in the

experiment were laid on the same day. This procedure was repeated the following day.

Strips were cut from the cups so that eggs would be submerged under water. A total of

30–50 eggs, from multiple cups, was placed in each rearing cage. Cages were 2L plastic

shoeboxes containing approximately 1L of deionized water. Cages were kept in a 14:10

light dark cycle in two environmental chambers; one set at 20�C and the other at 25�C.

These temperatures were chosen because they fall within the range of temperatures

(10–32�C) where California water striders are known to be actively reproductive (Fairbairn

and King 2009). After 24 h all unhatched eggs were removed such that a total of 27 cages

with 22–40 individuals per cage were assigned to each temperature. Juvenile water striders

were fed one frozen fruit fly per day per individual. Starting with the third instar 4–5 small

crickets per cage were added to the daily feeding regime. These were replaced with larger

crickets for the fifth instar.

Because live nymphs are delicate and difficult to measure, we estimated mean growth

rate per rearing temperature by sub-sampling individuals. Water striders have five larval

instars. We estimated age of each instar as the mean age of molting for that cage. To

estimate size at instar we collected 20–30 individuals per temperature 2 days after all

individuals had molted and preserved them in 70% EtOH. When water striders molted to

the adult instar we isolated males from females and winged (macropterous) individuals

from non-winged (apterous) individuals. Because non-winged morphs dominate most

populations (Fairbairn and King 2009) and the morphs differ in reproductive output

(Fairbairn 1988b) we used only non-winged animals to estimate reproductive allometry.

Twenty-four hours after isolating adults, each female was placed in her own cage along

with a strip of Styrofoam as a resting platform, half of a Styrofoam cup cut lengthwise as a

platform for laying eggs, and a non-winged male mate. Males were initially taken from a

stock tank to ensure that they were producing sperm before females were ready to begin

laying eggs. However, for females that molted later in the experiment we used males of the

same cohort that had molted a few days earlier. Thus for all pairs the male was initially

older and should have been producing mature sperm before females were ready to mate.

Five times throughout the experiment males within a laying temperature treatment were

collected, placed into a single container, then selected haphazardly to be placed back into

female cages to randomize any male effects on female fecundity. Adults were fed one

cricket each day and 5–10 flies every other day per pair with the previous days food

removed prior to each feeding. All surfaces were checked for eggs daily. Eggs were

counted then removed from rearing cages each day to determine daily laying rate per

female. Females were allowed to lay for 3 weeks after they first started to lay eggs, then

preserved in 75% EtOH.

Upon molting to the adult stage half of each temperature group was transferred to the

other temperature. This resulted in four combinations of rearing-laying temperatures

(20–20, 20–25, 25–20, and 25–25). We did this in order to separate the direct effects of

laying temperature from residual effects of rearing temperature. Size was estimated on

preserved water striders. A water strider was placed ventral-side up on a piece of KimWipe

laid over Styrofoam. She was then pushed up against a piece of glass to ensure that she lay

flat with legs stretched out to the sides. The water strider was then photographed with a

scale marked on the glass. Length measures were taken on the digital photos using tpsDIG

software (Rohlf 2008). Measures were limited to those that could be easily made on first

Evol Ecol (2012) 26:745–757 749

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instar larvae and included: head length, total body length, and length of femur for the

second and third legs. The first principal component of a PCA on these measures was used

as a general size measure.

Statistical analyses

The relationship between size and age was determined by comparing linear and several

non-linear regressions including quadratic, sigmoid, Gompertz, Logistic, and Von Berta-

lanffy models in SigmaPlot 10.0. The same was done for the relationship between body

size (as estimated by a PCA) and fecundity (mean egg production per day). The model that

best fit our data (highest adjusted r2 and lowest AIC) was used for further analysis.

Reproductive characters were compared using a two-factor analysis of variance with

rearing temperature and laying temperature as the independent factors. The size-fecundity

relationship was well represented by a linear regression so to test for differences in

reproductive allometry we compared average daily egg production for the four temperature

combinations with size as a continuous variable in a general linear model. Since we were

only interested in differences in the slopes of these relationships, only main effects and

two-way interactions were included.

Results

Two winged individuals were accidentally used in the experiment and these were removed

before analysis. A further 41 individuals either died or failed to produce eggs within

2 months of molting to the adult stage. These individuals were randomly distributed among

treatments (X2 = 5.73; df = 3; P = 0.13). These individuals were also excluded from

further analysis. In total 134 water striders laid eggs throughout the 3 week experimental

period and were included in the final analyses.

Growth and adult size

A sigmoid equation provided the best fit growth trajectory for both temperatures with

adjusted r2 [ 0.995 in both cases (Fig. 1). Females grew faster at 25� but molted to the

adult stage on average 25 days post-hatch as opposed to an average of 34 days for animals

Fig. 1 Growth trajectories for A.remigis reared at 20�C (opentriangle and dashed line) and at25�C (filled circle and solid line).Because we did not trackindividuals, ages represent meanages for each instar. Size is acomposite variable derived froma principal component analysison total length, head length, andlengths of the second and thirdfemur. Error bars are ± 1SD.Trajectories are based onSigmoid regressions (see text forequations)

750 Evol Ecol (2012) 26:745–757

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reared at 20�C. As a result, females reared at 25� were significantly smaller (F1,161 = 68.3,

P \ 0.001) and thus female water striders do follow the temperature-size rule over this

temperature range. Parameters and 95% confidence intervals for growth trajectories are

provided in Table 1a.

Reproductive characters

Water striders placed into 25�C cages following the adult molt started to lay eggs on

average 9.3 ± 0.67 (SEM) days later whereas those placed into 20�C took significantly

longer, on average 14.6 ± 0.69 (SEM) days (F1,138 = 29.12; P \ 0.001). The effect of

rearing temperature on this time period was not significant (F1,138 = 3.26; P = 0.07).

Most females did not lay eggs every day and the frequency depended upon both rearing

temperature (F1,128 = 4.87, P = 0.03) and laying temperature (F1,128 = 95.84, P \ 0.001)

with a significant interaction between the two (F1,128 = 7.45, P = 0.007). Females swit-

ched from 25 to 20�C had the fewest days with egg production (Fig. 2a). On days when

laying did occur, females laid fewer eggs at 20�C than at 25�C (F1,128 = 11.84, P \ 0.001)

but neither rearing temperature (F1,128 = 0.52, P = 0.47) nor the interaction between

temperatures (F1,128 = 0.48, P = 0.49) had a significant effect.

Cumulative egg production was consistent throughout the 21 days of laying for each

treatment (Fig. 2b). We therefore analyzed average laying rate (eggs/day for 3 weeks) as

our measure of fecundity (total eggs laid gave identical results). There was a modest effect

of rearing temperature on daily egg production with those reared at 20�C producing sig-

nificantly more than those reared at 25�C (F1,168 = 4.25; P = 0.04, Fig. 2c). This effect

was small in comparison to the effect of laying temperature (F1,168 = 57.79; P \ 0.001).

The interaction between rearing and laying temperature was not significant (F1,168 = 0.19;

P = 0.67).

The effect of rearing temperature on daily egg production appears to be largely due to

the size differences for when size was included as a continuous variable in a general linear

model, the effect of rearing temperature was no longer significant (F1,124 = 0.08;

P = 0.78). The main effect of laying temperature was still significant (F1,124 = 3.96; P =

0.048) but the slopes differed between laying temperatures (F1,124 = 4.68; P = 0.032,

Fig. 3). The interaction between size and rearing temperature was not significant

Table 1 Parameter estimates for (A) growth trajectories where size = b/(1 ? exp(-(age - t0)/k)), and(B) size-fecundity relationships where fecundity = m * size ? c for waterstriders reared under differentthermal regimes

(A) b t0 k

20�C 41.871 (41.153, 42.590) 18.367 (17.890, 18.845) 8.465 (8.178, 8.752)

25�C 39.692 (38.995, 40.388) 13.617 (13.291, 13.943) 5.972 (5.742, 6.201)

(B) Intercept (c) Slope (m) P

20–20�C -12.603 (-75.648, ?50.443) ?0.717 (-1.025, ?2.459) 0.404

25–20�C ?37.541 (-8.442, ?83.524) -0.760 (-2.096, ?0.576) 0.256

20–25�C -66.095 (-159.373, ?27.184) ?2.346 (-0.255, ?4.947) 0.076

25–25�C -52.302 (-108.944, 4.341) ?2.025 (?0.390, ?3.660) 0.017

Lower and upper 95% confidence values are given in parentheses

Evol Ecol (2012) 26:745–757 751

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(a)

(b)

(c)

Fig. 2 Reproductive data forwater striders (means ± 1SE).Open symbols in (a and c) are forfemales laying 20�C and filledsymbols are for females laying at25�C. Lines are drawn tohighlight potential interactioneffects between rearingtemperature and layingtemperature

752 Evol Ecol (2012) 26:745–757

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(F1,124 = 0.21; P = 0.65). Water striders laying at 20�C had a slope not significantly

different from zero (F1,72 = 0.03; P = 0.86) whereas those laying at 25�C showed a

positive relationship (F1,78 = 7.82; P = 0.007). Parameters and 95% confidence intervals

for the size-fecundity regressions are provided in Table 1b. Overall, temperature experi-

enced during growth had a modest effect on fecundity with a 3 week total of 327 eggs for

those reared at 20�C and a total of 303 eggs at 25�C, an 8% difference. Much more

dramatic was the effect of temperature experienced during egg production with totals of

374 eggs at 25�C and 255 eggs at 20�C, a difference of 47%.

Estimating optimal body size

Applying these data to the model of Arendt (2011) we can determine how reproductive

allometry should affect optimal adult body size. Here, we insert parameter estimates from

Table 1 into Eq. 9 to estimate the optimal body size for females spending their entire lives

at 25�C or at 20�C,

S25 ¼2:025� 39:692þ 5:972� 52:302� lj þ F

� �

2:025þ 5:972� 2:025� lj þ F� �

¼80:376þ 312:348� lj þ F

� �

2:025þ 12:093� lj þ F� �

and

S20 ¼0:717� 41:871þ 8:465� 12:603� lj þ F

� �

0:717þ 8:465� 0:717� lj þ F� �

¼30:022þ 106:684� lj þ F

� �

0:717þ 6:069� lj þ F� � :

We calculated optimal multivariate size for a range of values for lj ? F (Fig. 4). As

expected, the optimal size decreases as lj ? F increases (i.e., as juvenile mortality

increases) approaching an asymptote when this value exceeds one. Following Sibly and

Atkinson (1994), there is no region of this parameter space where it would be optimal to be

larger in the cold for spatial heterogeneity in temperature (lj ? F equal for both

Fig. 3 Relationship betweensize and fecundity for the fourtemperature treatments (growthtemperature-laying temperature).Solid regression lines are forthose where growth temperatureis the same as laying temperature.Dashed regression lines are forthose that were switched betweentemperatures. Thick lines arethose laying at 25�C and thinlines for those laying at 20�C

Evol Ecol (2012) 26:745–757 753

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temperatures), but it is just possible for this to be the case if juvenile mortality is very low

for 20�C and very high at 25�C (i.e., temporal heterogeneity where lj ? F is different

between temperatures). In both cases, the predicted optimal size, for all values of lj ? F, is

smaller than the actual sizes of 36.1 at 20�C and 34.6 at 25�C.

Discussion

Female A. remigis show a highly plastic growth and reproductive response to temperature.

This species follows the temperature-size rule in which those growing under cooler tem-

peratures mature later but at a larger size than those growing at a warmer temperature

(Atkinson 1994), at least for the temperatures tested. Rearing temperature had a modest

effect on fecundity, likely due to the larger size at maturation in the cold. Much more

dramatic was the effect of laying temperature with those laying at 25�C being 47% more

fecund than those laying at 20�C regardless of rearing conditions. Thus reproductive output

in A. remigis depends primarily upon the current conditions experienced by the female

rather than conditions experienced during juvenile stages.

Arendt (2011) suggested that reproductive allometry could compensate for the longer

time it takes to reach maturation in the cold. Thus being larger in the cold could be

adaptive if the relative gain in terms of reproduction, i.e., the slope of the size-fecundity

relationship, is greater in cold than in warm environments. Although slopes of the size-

fecundity relationship vary with temperature in A. remigis, the pattern is opposite to that

expected for a larger size in the cold to be adaptive. Thus reproductive allometry cannot

explain why A. remigis are larger when they grow up in cooler temperatures.

Clearly reproductive allometry cannot explain why water striders are larger when they

grow up under cooler conditions. Differences in juvenile mortality (Sibly and Atkinson

1994) can but only if the differences in mortality are very large. In fact, there is some

independent evidence that a smaller genetic size in the cold is favored by selection in

A. remigis and hence a larger phenotypic size in the cold probably is not adaptive. In

contrast to A. remigis, results from McCabe and Partridge (1997) on D. melanogaster are

Fig. 4 Effect of lj ? F onoptimal multivariate body size.Lines with symbols are calculatedoptimal body sizes for 20�C(open triangle with dashed line)and 25�C (filled circle with solidline). Lines without symbols aremean realized sizes for 20�C(dashed line) and 25�C (solidline)

754 Evol Ecol (2012) 26:745–757

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consistent with the predictions of Arendt (2011). In addition, populations of D. melano-gaster from colder, high latitude populations are genetically larger than those from war-

mer, low latitude populations (De Moed et al. 1997; Azevedo et al. 1998). When

populations have evolved to show the same pattern as phenotypic plasticity, this is called

cogradient variation (Conover and Schultz 1995). In this case, it indicates that a larger

body size in the cold is adaptive for D. melanogaster. By contrast, A. remigis follow the

converse of Bergmann’s rule (Blanckenhorn and Fairbairn 1995; Brennan and Fairbairn

1995). That is, those from warmer, lower latitudes are larger than those from cooler, higher

latitude populations except in areas where populations transition from bivoltine to uni-

voltine life cycles (Brennan and Fairbairn 1995). This is explained by the shorter growing

season at higher latitudes (Blanckenhorn and Demont 2004) and the same pattern has been

demonstrated in streams only 6 km apart but differing in average temperature (Blanc-

kenhorn 1991a). Because the evolved pattern is the reverse of the plastic pattern in body

size, this is called countergradient variation (Conover and Schultz 1995) and indicates that

a larger body size in the cold is likely to be maladaptive.

Atkinson (1996) and Angilletta et al. (2004) both argued that there is unlikely to be one

single explanation for all instances of the temperature-size rule. In some cases the phe-

notypically plastic production of a larger body size in the cold may be an adaptive response

to difference in mortality rates or reproductive allometry, or it may reflect thermal con-

straints on growth and development. Despite the abundance of potential explanations for

this pattern, there have been relatively few empirical studies to test any of them. Here, we

have shown that a larger body size in the cold cannot be explained by reproductive

allometry in the water strider A. remigis. Furthermore, because A. remigis shows count-

ergradient variation with respect to temperature in the wild, it is likely that the plastic

response is not adaptive. We suggest known countergradient and cogradient patterns

(Conover and Schultz 1995) may be useful in identifying cases where the temperature-size

rule is likely to be maladaptive and adaptive (or at least neutral), respectively.

Acknowledgments Thanks to Matthew Wolak for his invaluable help with the water striders and theadvice of two anonymous reviewers which greatly improved the clarity of this paper. This work wassupported by NSF grant DEB-0743166 to D.F.

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