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Proc. R. Soc. B (2011) 278, 2265–2273
doi:10.1098/rspb.2010.2479
Published online 5 January 2011
Adaptation to climate change: contrasting
patterns of thermal-reaction-norm evolution
in Pacific versus Atlantic silversides
Hannes Baumann* and David O. Conover
School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, NY 11794-5000, USA
How organisms may adapt to rising global temperatures is uncertain, but concepts can emerge from
studying adaptive physiological trait variations across existing spatial climate gradients. Many ectotherms,
particularly fish, have evolved increasing genetic growth capacities with latitude (i.e. countergradient variation (CnGV) in growth), which are thought to be an adaptation primarily to strong gradients in
seasonality. In contrast, evolutionary responses to gradients in mean temperature are often assumed to
involve an alternative mode, ‘thermal adaptation’. We measured thermal growth reaction norms in Pacific
silverside populations (Atherinops affinis) occurring across a weak latitudinal temperature gradient with
invariant seasonality along the North American Pacific coast. Instead of thermal adaptation, we found
novel evidence for CnGV in growth, suggesting that CnGV is a ubiquitous mode of reaction-norm evolution
in ectotherms even in response to weak spatial and, by inference, temporal climate gradients. A novel, largescale comparison between ecologically equivalent Pacific versus Atlantic silversides (Menidia menidia)
revealed how closely growth CnGV patterns reflect their respective climate gradients. While steep growth
reaction norms and increasing growth plasticity with latitude in M. menidia mimicked the strong, highly
seasonal Atlantic coastal gradient, shallow reaction norms and much smaller, latitude-independent growth
plasticity in A. affinis resembled the weak Pacific latitudinal temperature gradient.
Keywords: countergradient variation; growth capacity; conversion efficiency; latitudinal gradients;
temperature; seasonality
1. INTRODUCTION
The need to understand how organisms adapt to climatic
variability has increased with the evidence for unprecedented global climate change [1]. Because temperature
greatly influences the expression and fitness of many
phenotypic traits, adaptive landscapes will be altered
substantially by long-term changes in mean temperature
and seasonality [2]. Anticipating evolutionary responses
to climate change remains a complex challenge. Retrospective analyses or other temporal approaches are often
inconclusive owing to a lack of replication and difficulties
in distinguishing genetic from plastic responses [3,4].
An alternative is to study adaptations to climate change
across spatial scales among extant populations. Many
species occur across temperature and seasonality clines
along latitudinal, altitudinal, depth or continentality gradients, and exhibit apparent adaptive variations in
morphological and physiological traits [5]. Spatial climate
gradients provide opportunities to rigorously identify
mechanisms of adaptation that, by analogy, may elucidate
evolutionary responses to temporal climate change.
One form of spatial adaptation that has gained strong
empirical support across taxa is countergradient variation
(CnGV; reviewed by [6]). CnGV occurs when genotypes
with a higher (or lower) value for a given trait are predominantly found in environments that tend to decrease
(or increase) the trait’s phenotypic value (figure 1). The
* Author for correspondence ([email protected]).
Electronic supplementary material is available at http://dx.doi.org/
10.1098/rspb.2010.2479 or via http://rspb.royalsocietypublishing.org.
Received 12 November 2010
Accepted 7 December 2010
most common form of CnGV involves metabolic compensation and is displayed mostly in physiological traits,
for example, in the genetically higher growth capacities
of many poikilotherms at high versus low latitudes
(e.g. [7] (Reptilia); [8] (Pisces); [9] (Insecta); [10]
(Gastropoda); [11] (Amphibia)). In cases of CnGV in
growth, genetic growth capacities are adjusted upward
or downward over a species’ entire viable temperature
range, with thermal reaction norms (¼temperaturespecific phenotypic trait expressions, figure 1) shifted in
parallel to higher or lower levels. This mode of adaptation
is currently interpreted as an evolutionary response to
gradients in seasonality, i.e. the degree of seasonal temperature fluctuations influencing the length of the growing
season [6,12,13]. However, latitudinal adaptations could
also evolve without changing the overall growth capacity
but via shifts in thermal reaction norms toward a higher
or lower range of temperatures in accordance to those
most often experienced in nature [14]. In this case, thermal reaction norms would cross (figure 1) and represent a
form of genotype environment interaction rather than
CnGV [15]. Such thermal adaptation is thought to be
the primary adaptive response to gradients in mean
temperature [15,16]. However, this distinction is still
uncertain, as it remains largely based on studies that
examined trait variations in single species and across
single latitudinal gradients where mean temperature
and seasonality varied concomitantly (e.g. along the
North-American Atlantic coast [8,15,17]). Hence, the
confounding effects of mean temperature versus seasonality as agents of selection have yet to be disentangled.
This uncertainty could be effectively addressed by a
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H. Baumann & D. O. Conover
trait (e.g. growth capacity)
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1
Growth adaptations to climate change
2
temperature
Figure 1. Schematic diagram of two alternative modes of
thermal reaction norm evolution across thermal gradients
such as those across latitudes. Consider the thermal reaction
norm (i.e. the trait expression at a range of temperatures) of a
hypothetical organism adapted to some average temperature
regime (blue curve). A shift to lower average temperature
conditions (e.g. at higher latitudes) may lead to ‘thermal
adaptation’, i.e. a horizontal shift in the reaction norm and
a new lower thermal optimum (1, black curve). This results
in crossing reaction norms of different populations reared in
common garden environments. Alternatively, local adaptation may involve CnGV, which leads to genetic increases
in trait expression over the entire range of experienced temperature without changing the thermal optimum (2, red curve;
population reaction norms do not cross).
large-scale comparative approach using latitudinal gradients that differ substantially in their seasonality and
temperature change.
Consider, for example, the highly contrasting latitudinal temperature and seasonality gradients that exist along
the North American Atlantic versus Pacific coast [18]. We
quantified this contrast by extracting mean coastal
sea surface temperatures (SST) per week and degree latitude from a publicly available dataset of in situ and
satellite observations (http://dss.ucar.edu/datasets/ds277.
0, 1982 – 2008, figure 2). Between 278 N and 498 N, the
absolute magnitude of temperature fluctuations along
the Atlantic coast is twice as large (20.98C to 29.38C,
DTAtl ¼ 30.28C) as on the Pacific side (7.6 –22.08C,
DTPac ¼ 14.48C). On average, mean temperatures
decrease almost three times faster with latitude along
the Atlantic (21.118C per latitude) than on the Pacific
coast (20.408C per latitude). Seasonality, i.e. the
latitude-specific maximum summer – winter difference,
is small and independent of latitude along the
Pacific coast (2.6– 6.78C), but strong and increasing
with latitude along the Atlantic coast, particularly
north of Cape Hatteras (DTAtl 28.58 N ¼ 6.38C, DTAtl
45.58 N ¼ 18.68C, figure 2).
We used these two gradients to contrast latitudinal
growth adaptations between two broadly distributed, ecologically equivalent atherinopsid fish species: Pacific
topsmelt (Atherinops affinis) and the Atlantic silverside
(Menidia menidia). To reveal extant genetic variation
in growth capacity and efficiency, A. affinis offspring
from four different populations were reared in common
garden experiments similar to those published previously
for M. menidia [8,19]. Given the small Pacific temperature gradient with its relatively invariant seasonality, we
Proc. R. Soc. B (2011)
expected A. affinis latitudinal growth adaptations to be
either undetectable or occur via shifts in thermal optima
of growth capacity (crossing thermal reaction norms,
figure 1). Instead, we found novel evidence for CnGV,
i.e. higher growth capacities with increasing latitude over
the entire thermal range of A. affinis. While CnGV thus
appears to be the prevalent mode of thermal-reactionnorm evolution even across simple temperature gradients
(Pacific coast), a strong seasonality gradient (Atlantic
coast) probably necessitates additional adaptive increases
in growth plasticity in high-latitude populations.
2. MATERIAL AND METHODS
(a) Study species
Menidia menidia and A. affinis are two silverside species
(Atherinopsidae) that occur over a broad and similar latitudinal range along the Atlantic and Pacific coast, respectively
(M. menidia: 30– 468 N [8]; A. affinis: 24– 458 N [20]).
Both are estuarine, schooling, omnivorous fish of equivalent
trophic levels. Both are multiple batch spawners laying
benthic, intertidal eggs on a semilunar cycle mainly between
spring and summer [21,22]. In M. menidia, onset and length
of the spawning season shift with latitude, while the same is
not known for A. affinis. Both species mature and spawn at
age 1 but differ in their maximum size and age: M. menidia
is essentially an annual silverside, reaching as much as
15 cm in total length with less than 1 per cent of fish reaching
age 2 [21], while A. affinis reaches up to 37 cm and typically
lives to ages 4–5 [23].
(b) Atherinops affinis offspring collection
Fertilized A. affinis eggs were collected by strip-spawning
ripe adults caught with beach seines in four Pacific estuaries.
For the first year of experiments (2008), populations P2338 N,
P3378 N and P4438 N were sampled, whereas in the second year
(2009), populations P1288 N, P2338 N and P3378 N were
sampled (table 1). Re-sampling of P2338 N and P3378 N was
done to facilitate inter-annual comparisons. Sufficient genetic diversity representative of each population was
assumed after strip-spawning at least 20 individuals of each
sex. To transfer embryos to our laboratory facility at Flax
Pond (Stony Brook University, Long Island, NY, USA),
screens with attached egg masses were wrapped in moist
paper towels and stored in common thermos cans. Upon
arrival, eggs were placed in aerated 20 l containers sitting
in large (700 l) temperature-controlled baths at three
(i.e. 15, 21, 278C in 2008) or four (15, 21, 24, 278C in
2009) temperature treatments. Containers were equipped
with screened holes to ensure water exchange with the
baths. The photoperiod was 15 L : 9 D. A salinity of 30 +
2 psu was maintained during both years using water drawn
from saline ground wells. Addition of commercial sea salt
(Instant Ocean) allowed controlling for variation in salinity
among years. Depending on the temperature, A. affinis
larvae hatched 6 –16 days post-fertilization at approximately
6 mm (population independent) and were start-fed with a
mix of larval powder food (Otohime Marine Weaning Diet,
size A, Reed Mariculture) and newly hatched brine shrimp
nauplii (Artemia salina, San Francisco strain, Brine Shrimp
Direct, Inc.).
Growth capacity, i.e. the temperature-specific growth rate
at unlimited feeding conditions, was measured during the
first experimental period. Trials started 4–13 days
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Growth adaptations to climate change H. Baumann & D. O. Conover
(a)
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(b)
Cape Flattery
(48.4° N)
Cape North,
Nova Scotia
(47.1° N)
47.5° N
38 wk
0
43.5° N
15
12
12
10
16 wk
45.5° N
3
18
21
25 wk
41.5° N
52 wk
39.5° N
15
52 wk
3
6
12
15 8
1
33.5° N
29.5° N
27.5° N
5
10 15 20 25 30 35 40 45 50
week of year
Cape Hatteras
(35.2° N)
52 wk
31.5° N
18
Pt. Eugenia
Baja California
(27.8° N)
35.5° N
9
21
24
15
37.5° N
24
Monterey
(36.5° N)
Pt. Conception
(34.4° N)
27
12
Cape Cod
(41.8° N)
5
10 15 20 25 30 35 40 45 50
week of year
°C
Vero Beach
(27.6° N)
–1 1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
Figure 2. Contour representation of latitude-specific, weekly mean SSTs along the (a) Pacific and (b) Atlantic coast, derived
from long-term SST data (1982–2008). For every 18 of latitude, data from the grid cell next to land in the land-sea mask were
used. For orientation, geographical reference points are given next to each panel. Grey lines and values denote the number of
weeks per year, when average temperature conditions are above the growth permitting thermal threshold in Pacific (108C) and
Atlantic silversides (128C).
Table 1. Atherinops affinis sampling sites and dates during the two experimental years.
estuary, site, state
location
sampling date(s)
acronym
Laguna Manuela, northern arm, Baja California, MX
28.258 N
114.088 W
32.578 N
117.138 W
36.828 N
121.748 W
43.388 N
124.208 W
April 2009 (22– 24)
P1288 N
May 2008 (19)
May 2009 (11)
May 2008 (16 and 17)
May 2009 (7 –9)
June 2008 (19)
P2338 N
Tijuana estuary, Oneonta Slough, California, USA
Elkhorn Slough, South Marsh, California, USA
Coos Bay, North Bend, Oregon, US
post-hatch after larvae had reached a mean + s.d. total length
(TL) of 8.0 + 0.9 mm (measured to the nearest 0.1 mm via
calibrated digital pictures and ImagePro software). A
random sample of 10–20 larvae per temperature/population
was measured for initial TL and wet weights (W, nearest
0.1 mg, Mettler AE163), followed by randomly placing
35 + 2 larvae in each of three replicate containers (20 l)
per temperature/population. Fish were subsequently reared
on ad libitum rations of newly hatched brine shrimp nauplii
until reaching a mean + s.d. TL of 23.2 + 2.1 mm (consistent with [8,15]). At this point, a sub-sample of at least 10 fish
per container was measured for TL (0.1 mm, using callipers)
and W (same scale). During the first 3 days of each trial, dead
specimens were replaced to correct for initial mortality owing
to handling. Total mortality was low, averaging 4.2 (2008)
and 2.3 fish per replicate (2009). Growth capacity in length
(mm d21) and weight (dimensionless) was calculated for
each replicate by dividing the difference in mean TL and
W (cube-root transformed) by the corresponding duration
of the first experimental period (i.e. 18–80 days).
Dry weight-based food consumption and conversion
efficiency (¼ the increase in body mass per unit food
ingested, %) was assessed during the second experimental
Proc. R. Soc. B (2011)
P3378 N
P4438 N
period, when the remaining fish grew at excess feeding conditions from 23.2 mm TL (see above) to an average (+s.d.)
of 32.5 + 2.7 mm TL. The number of remnant nauplii was
estimated daily by taking three 5 ml water samples from each
container and counting all live nauplii in each using Bokorov
chambers and a dissecting microscope. Nauplii added to containers were similarly quantified by counting sub-samples
from nauplii hatching cones. The method had an estimated
average precision of 20.9 per cent (CV). Daily nauplii consumption per container, i.e. remaining þ added nauplii on
any given day minus nauplii remaining on the following day,
was then converted to dry weights (dW ) using a value of
2.1 mg nauplius21 consistent with Present & Conover [19].
Fish W was converted to dW using the relationship
dW ¼ 0.0706 W 1.2046 (r 2 ¼ 0.997, p , 0.001, n ¼ 56)
derived from a representative sub-sample that was ovendried at 658C for 98 h. Mean daily consumption estimates
(% body dW ) were scaled by the daily mean dW of all fish in
each replicate, derived via calculating a mean dW growth
rate of each replicate during the second period. Food conversion efficiency (%) was calculated for each replicate as the
mean total increase of all fish dW during the second period
relative to the total dW of consumed nauplii.
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H. Baumann & D. O. Conover
Growth adaptations to climate change
(c) Minimum temperature permitting juvenile growth
To determine the lowest growth-permitting temperature in
A. affinis, some excess juveniles from reservoir containers in
2009 were reared at ad libitum rations of brine shrimp nauplii at 128C, 108C, and 88C for four to five weeks. Prior to
each trial, 30 juveniles of similar size were randomly assigned
to each of three (128C) or two replicates (108C, 88C) per
population and acclimatized for 5– 6 days to target temperature and excess food. Trials started by sacrificing a random of
10–12 fish for initial W measurements and ended 25–38
days later by determining W of all remaining specimens.
Mean W of initial and final samples were tested for significant differences by t-tests. Average mortality was less than
one fish per replicate.
(d) Menidia menidia growth capacity and efficiency
We used original data from two analogous common garden
experiments conducted at the same laboratory facility with
identical culturing equipment [8]. Laboratory-spawned offspring from three populations originating from South
Carolina (SC328 N), New York (NY418 N) and Nova Scotia
(NS448 N) were reared over a similar larval size range
(7–18 mm TL) on excess brine shrimp nauplii and at four
replicated temperatures (17, 21, 28, 328C). Estimates of
M. menidia food consumption and conversion efficiencies
were derived from slightly smaller fish than A. affinis, monitored either individually over 24 h (consumption) or in small
groups over 5 days (efficiency) as described in Present &
Conover [19].
Statistical analyses were conducted in SPSS Statistics 17.0
(SPSS, Inc.) using replicate means (containers) as individual
statistical entities. Growth capacities (length, weight), food
consumptions and conversion efficiencies were first tested for
significant (p , 0.05) effects of temperature using separate
analyses of variance (ANOVA) per year and population. Likewise, population effects were assessed through ANOVAs per
year and temperature. Least-significant difference (LSD) or
Dunnet-T3 post hoc tests were used in case of homogeneous
or heterogeneous variances between groups, respectively. For
growth capacities (GC, length, weight), data from both years
were used to construct general linear models (LM) of the
form GC ¼ T þ P þ T P þ Y þ e to test for significant overall effects of temperature (T ), population (P), temperature population interaction and year (Y, e ¼ error).
3. RESULTS
(a) Atherinops affinis thermal reaction norms
In both years, growth capacity significantly increased with
temperature and from southern to northern populations
(13 separate ANOVAs, p , 0.05, figure 3a,b). In 2008,
the P4438 N population grew on average 0.30, 0.55 and
0.76 mm d21 at 15, 21 and 278C, respectively, which
was significantly faster than the P3378 N (LSD, p ,
0.001) and P2338 N populations (LSD, p , 0.001). Population growth differences of about 0.05 mm d21 remained
similar across experimental temperatures in the first year
(i.e. temperature population interaction term not significant, LM, F4,26 ¼ 1.09, p ¼ 0.39, figure 3a). During
the second year, P3378 N fish again grew significantly
faster at all temperatures than P2338 N (Dunnet-T3, p ,
0.05), which in turn grew faster than those from P1288 N
(Dunnet-T3, p , 0.05). Second year growth rates were
7– 26% higher in the repeated P2338 N and P3378 N
Proc. R. Soc. B (2011)
populations. There was also a weak but significant
temperature population interaction (LM, F6,35 ¼ 4.07,
p ¼ 0.006), mainly due to steeper growth capacity
increases with temperature in the P3378 N population
(figure 3b). The 248C treatment proved meaningful in
revealing the general nonlinearity of the A. affinis
growth reaction norm, suggesting 278C to be close to
the thermal growth capacity maximum of A. affinis. Initial
trials at 128C and 308C failed owing to poor hatching success and near total mortality of larvae within the first few
days, thus indicating the thermal tolerance limits of the
youngest A. affinis life stages. Patterns in weight growth
were the same as those described for length. Overall, an
LM with data from both years returned statistically significant effects (p , 0.001, electronic supplementary material,
table S1) of temperature, population and year with a weak
temperature population interaction (p ¼ 0.017).
In both years, weight-specific food consumption
increased significantly with temperature (ANOVA,
F(2008)2,24 ¼ 8.7, p , 0.001; F(2009)3,32 ¼ 42.0, p ,
0.001) from daily mean values of 21 – 39% body dW at
158C to 45 – 53% body dW at 278C (electronic supplementary material, figure S1a,b). However, there were
no significant differences between populations, except for
lower values of P4438 N at 158C compared with P3378 N
and P2338 N (ANOVA, F(158C)2,6 ¼ 27.6, p ¼ 0.01).
In both years, food conversion efficiencies showed a
tendency to increase with latitude, however, data were
very heterogeneous and most differences non-significant
(electronic supplementary material, figure S1c,d).
In 2008, P4438 N converted on average 16, 20 and 17
per cent of consumed food into weight at 15, 21 and
278C, respectively; values that were 5 per cent higher
(ANOVA, d.f. ¼ 2, p , 0.05) than P3378 N and P2338 N
efficiencies (electronic supplementary material, figure
S2c). The two repeated populations showed significantly
(ANOVA, d.f. ¼ 1, p , 0.05) higher conversion efficiencies in the second year at 158C and 218C (electronic
supplementary material, figure S2d ) consistent with the
observed overall increase in growth rates. For P2338 N
and P3378 N, highest mean efficiencies of 21.2 and 24.6
per cent occurred at 248C, while P1288 N values peaked
at 218C (electronic supplementary material, figure S2d ).
(b) Juvenile growth at low temperatures and
unlimited food
At 128C, juveniles from the three populations tested
(P1288 N, P2338 N, P3378 N) grew in mean weight, although
increases were only significant (t-test, p , 0.01, table 2)
for the two northernmost populations. At 108C, weight
changes were still positive, but not significantly different
from zero. At 88C, both P1288 N replicates and one of
two P2338 N replicates showed slight weight losses, while
weight in P3378 N did not change significantly (table 2).
(c) Atlantic compared with Pacific patterns of
CnGV in growth capacity
Both in M. menidia and A. affinis, latitudinal growth
adaptations were achieved via increases in growth capacity
across all temperatures from low- to high-latitude populations, not by intra-specific horizontal shifts in thermal
reaction norms. Still, reaction norms differed greatly
between species but the divergence was owing to the
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Growth adaptations to climate change H. Baumann & D. O. Conover
(a)
2269
(b)
growth capacity (TL, mm d–1)
0.9
0.8
0.7
0.6
0.5
0.4
0.3
0.2
15
18
21
24
temperature (°C)
27
15
18
21
24
temperature (°C)
27
Figure 3. Atherinops affinis. Thermal reaction norms of growth capacity in offspring from four populations along the US and
Mexican Pacific coast, as revealed by common garden experiments in (a) 2008 and (b) 2009. Lines intersect means +1 s.e. For
clarity, means are slightly jittered along the x-axis. Dash-dotted line: P1288 N (Laguna Manuela), solid line: P2338 N (Tijuana
estuary), dashed line: P3378 N (Elkhorn Slough), dotted line: P4438 N (Coos Bay).
much greater increase in thermal growth plasticity with
increasing latitude in M. menidia. When averaged across
populations, M. menidia growth capacity increased from
0.32 mm d21 (178C) to 1.12 mm d21 (288C), which corresponds to an average slope of 0.074 mm d218C21 or a
Q10 of 3.12 (electronic supplementary material, figure
S2a). In contrast, average A. affinis growth capacities
increased only from 0.26 mm d21 at 158C to
0.78 mm d21 at 278C, corresponding to a much smaller
slope of 0.043 mm d218C21 (Q10 ¼ 2.49, P4438 N values
adjusted for year effect). More importantly, the slopes
of growth reaction norms were relatively similar between
A. affinis populations, but differed greatly between M.
menidia populations, thus causing the temperature population interaction term to be very strong in Atlantic
but relatively weak in Pacific silversides. Menidia menidia
from SC328 N grew 0.29 – 0.88 mm d21 (17 – 288C),
while those from NS448 N grew 0.33 –1.36 mm d21 (17 –
288C), which means a doubling in slopes from 0.049 to
0.098 mm d218C21. In contrast, southernmost A. affinis
(P1288 N) grew 0.20– 0.66 mm d21 (15 –278C), while
northernmost P4438 N grew 0.33– 0.90 mm d21 (15 –
278C, adjusted for year effect), corresponding to similar
slopes of 0.038 and 0.048 mm d218C21, respectively.
Food consumption and conversion efficiency of
M. menidia increased more strongly with temperature and
latitude than in A. affinis (electronic supplementary material,
figure S2b, [19]). Southernmost M. menidia had average
efficiencies of 12.5 and 21.3 per cent (at 17 and 288C,
respectively) that were comparable to values observed in A.
affinis. Efficiencies beyond 30 per cent, on the other hand,
as measured in northernmost M. menidia at 288C, were considerably above all A. affinis estimates. However, the general
heterogeneity of both datasets and slightly differing experimental protocols place limitations on consumption/
efficiency comparisons between the two species.
4. DISCUSSION
This study determined thermal growth reaction norms of
Pacific silverside populations to test the paradigm that
Proc. R. Soc. B (2011)
species distributed across simple temperature gradients
evolve local adaptations via shifting thermal growth
optima towards each population’s average temperature
experience (i.e. ‘thermal adaptation’, figure 1). Instead,
we found that Pacific silversides evolved CnGV in
growth (figure 1), an alternative mode of reaction norm
evolution previously assumed to be an adaptation to
strong seasonality gradients (e.g. in Atlantic silversides
[15]). If CnGV is the prevalent adaptive mechanism
across simple temperature gradients in space, it probably
plays an important role, too, for adaptations in time
across thermal gradients, such as those elicited by
global warming. In addition, our novel coast-to-coast
comparison has broadened the current understanding
about CnGV by suggesting a strong link between the
characteristics of latitudinal climate gradients and the
different, corresponding CnGV patterns in reaction
norm evolution.
(a) Latitudinal growth adaptation in Pacific
silversides
Our results clearly indicated CnGV in growth capacity
among populations of A. affinis, thereby documenting
the first case of growth CnGV in a coastal Pacific fish.
Thermal reaction norms in growth capacity were generally parallel and differed primarily in elevation, with
more northern populations growing faster than those
from the south. Because mean growth capacity changed
in rank order with latitude, this pattern of variation is
probably the outcome of natural selection, not random
genetic drift [5]. This suggests that sub-maximal growth
capacities are adaptive, probably because evolutionary
incentives for maximizing body size are countered by
physiological trade-offs of fast growth [6], with the
balance being temperature- and therefore latitudedependent. Selection for increased body size via faster
growth follows from survival advantages during the early
life stages of fish known as ‘bigger-is-better’ or ‘stageduration’ paradigms [24 – 26]. In many fishes, larger
body size also increases juvenile survival during the first
winter [27 – 29] and confers higher fertility during
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H. Baumann & D. O. Conover
Growth adaptations to climate change
Table 2. Atherinops affinis. Growth of juveniles (45 –50 mm TL) at low temperatures and unlimited food. Average fish wet
weights (g) at the beginning (Wini) and end (Wend) of trials at 12, 10 and 88C, and trial lengths are given per replicate.
Italicized pairs denote weight loss, bold pairs with asterisks denote significant weight changes (t-test).
88C
108C
128C
population
replicate
Wini – Wend (g)
days
Wini –Wend (g)
days
Wini – Wend (g)
days
P3378 N
1
2
1
2
3
1
2
3
0.57 –0.64
0.58 –0.60
0.66 –0.77
0.70–0.64
—
1.04 –0.78**
0.91–0.83
—
25
25
25
25
—
25
25
—
0.53 –0.61
0.56 –0.61
0.70 –0.70
0.67 –0.70
—
0.78 –0.81
0.75 –0.84
—
26
26
26
26
—
26
26
—
0.49 –0.73**
—
0.43 –0.61**
0.46 –0.61**
0.48 –0.68**
0.39 –0.46
0.44 –0.51
0.45 –0.57
28
—
38
38
38
32
32
32
P2338 N
P1288 N
*p , 0.05.
**p , 0.01.
adulthood [30]. Trade-offs of fast growth, on the other
hand, include smaller activity scopes and thus poorer burst
and routine swimming of faster compared with slower growing fish of the same size [31–33], which implies higher
predation vulnerabilities for fast growers [34–36]. The present findings for A. affinis suggest that the countervailing
selection pressures on growth capacity operate even across
latitudinal scales where the change in mean temperature is
very small. For example, mean annual temperature differed
by as little as 1.28C between our Pacific study sites
(figure 4c), but still evoked detectable shifts in growth
capacity. The existence of CnGV in Pacific silversides therefore indicates that growth is finely tuned to local selection
pressures even across modest changes in climate.
Growth capacity variations necessitate changes in either
food consumption, conversion efficiency or both, yet physiological efficiencies within a species are often assumed to
become maximized by natural selection [37,38]. Common
garden experiments on vertebrate and invertebrate species
have challenged that notion by finding higher food consumptions and higher conversion efficiencies in faster
growing, higher latitude populations (e.g. [19,39,40]).
Our data for A. affinis also showed higher conversion efficiencies in northern compared with southern populations.
Changes in consumption were not evident, either because
the small magnitude of A. affinis growth CnGV did not
require them or because the differences were masked by
the large uncertainty of our nauplii counting method.
Overall, this study supports the notion that sub-maximal
growth rates in fish involve sub-maximal growth efficiencies, either because directional selection for maximizing
efficiency is weak or because high efficiencies are associated with so far unknown trade-offs, related or
conceptually similar to the trade-offs of fast growth.
(b) Countergradient growth variation across
different gradients
When comparing Pacific with Atlantic silversides, it is relevant that the same general mode of latitudinal growth
adaptation, CnGV, has evolved despite such contrasting
gradients in climate. Although mean temperature
decreases with latitude along both coasts, the Atlantic
gradient is three times steeper than the Pacific temperature gradient. Moreover, seasonality, i.e. the degree of
seasonal temperature fluctuations, changes greatly with
Proc. R. Soc. B (2011)
latitude along the Atlantic coast, while being latitudeindependent along the Pacific coast (figure 4c,d).
Evidence for growth CnGV in Pacific silversides suggest
that this form of adaptation can evolve in response to
changes in mean temperature alone, independent of
changes in seasonality [8,17].
In M. menidia, size-selective overwinter mortality acts as
a strong agent of selection in driving the evolution of CnGV
in growth [12,15]. In many species with distributions across
large seasonality gradients, growth is limited to a fraction of
the year when temperatures exceed a species-specific
threshold (e.g. 128C [8]). In Atlantic silversides, this results
in a threefold decrease in growing season length from
southern- to northernmost populations (figure 2b), yet a
reduction in body size is penalized by the increasingly
severe and size-selective winter mortality in latitudes
above approximately 368 N ([28,41] figure 4d). In contrast,
winter mortality is unlikely to be responsible for growth
CnGV in Pacific silversides, because ambient temperatures
would permit year-round growth if food is not a constraining factor (figure 2). Ad libitum-fed juveniles in our
experiments were able to sustain growth above 108C.
Temperatures exceeding this threshold occur year-round
in coastal Pacific waters south of 458 N (figures 2 and 4c).
Other studies have documented latitudinal growth CnGV
in fish species, where size-selective winter mortality
is equally unlikely (e.g. M. peninsulae [15]). Hence, sizeselective winter mortality is not necessary to trigger the
evolution of CnGV in growth rate.
Even though CnGV is the common mode of adaptation
in both species/coasts, the norms of reaction differed
greatly in a manner that reflected the gradients in which
they evolved. Average growth plasticity is much greater in
Atlantic than Pacific silversides, resulting in a two-fold
difference in average slopes of reaction norms between
the two species. This coincides with the steeper latitudinal
decrease in mean temperature along the Atlantic than the
Pacific coast (figure 4). More importantly, growth plasticity increases greatly from southern to northern Atlantic
silverside populations but remains similar between Pacific
silverside populations. This mimics the presence versus
absence of a latitudinal seasonality gradient along the
Atlantic versus Pacific coast (figures 2 and 4). Northern
populations of M. menidia must accelerate their growth
rate rapidly with temperature in order to compensate for
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Growth adaptations to climate change H. Baumann & D. O. Conover
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0
15 17 19 21 23 25 27 29 31
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temperature (°C)
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no growth
no growth
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Figure 4. Correspondence of latitudinal growth adaptations in (a) Pacific and (b) Atlantic silversides to large-scale climate gradients
along the (c) Pacific and (d) Atlantic coast. (a,b) Population-specific colour shading depicts areas between 10th and 90th percentiles
of temperature-specific growth capacity, calculated from combined data by dividing the percentile differences in TL before and after
each growth trial by its duration (days). P4438 N data were adjusted for year effect. (c,d) Colour shading depicts areas between average
long-term annual minima (winter) and maxima (summer) of temperature per 18 latitude along the Atlantic and Pacific coast. The
characteristic mid-latitude depression in Pacific summer temperatures coincides with the extent of the California Current upwelling
system [51]. Dotted lines denote the latitudinal origin of investigated silverside populations, solid lines depict the thermal threshold of
species-specific growth potentials (A. affinis: 108C; M. menida: 128C). (a) Pacific—Atherinops affinis, red lines/area, P1288 N; green
lines/area, P2338 N; blue lines/area, P3378 N; black lines/area, P4438 N. (b) Atlantic—Menidia mendia, red lines/area, SC328 N; green
lines/area, NY418 N; blue lines/area, NS448 N.
the thermally constrained growing season at higher latitudes ([8], figure 2). The greater acceleration of growth
capacity with temperature in northern Atlantic silversides
might therefore be the result of additive selection forces,
i.e. those generally compensating for latitudinal decreases
in mean temperature plus those compensating for the
decrease in growing season.
We conclude that small latitudinal gradients in mean
temperature are sufficient to elicit adaptive CnGV in Pacific silversides, which display parallel growth reaction norms
across latitudes. In contrast, Atlantic silversides display
much higher plasticity in growth and also increased plasticity at higher latitudes. It is the plasticity of growth that
represents adaptation to highly seasonal environments
driven by the size-selectivity of winter mortality. Thus, seasonality gradients have a strong magnifying effect on
thermal growth plasticity of high-latitude populations.
These conclusions are not restricted to fish, but probably
shape local adaptation patterns in other vertebrate and in
Proc. R. Soc. B (2011)
invertebrate taxa in a similar way. Metabolic compensation
via CnGV is equally prominent in amphibians [11], molluscs [10] and insects [9,40,42], hence gradient effects
should also be evaluated across taxa, e.g. by a meta-analysis
of all published cases of growth CnGV.
Noteworthy constraints of our approach include, first,
its focus on a brief early period in both species life
cycle. While growth differences in Atlantic silversides are
known to persist until adult life [43], this is not known yet
for Pacific silversides, although growth differences in our
experiment persisted well beyond the reported growth
interval (until approx. 4–5 cm TL; H. Baumann 2010,
unpublished data). Second, it is not known yet for A.
affinis, how traits like growth rate or body size vary phenotypically in the wild, hence, whether the genetic differences
partially compensate, equalize or overcompensate for
latitudinal temperature differences. Third, comparing
the Pacific (weak-temperature/no-seasonality) with the
Atlantic gradient (strong-temperature/strong-seasonality),
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2272
H. Baumann & D. O. Conover
Growth adaptations to climate change
and contrasting two species (even if ecologically and
taxonomically equivalent) is inevitably imperfect from a
strict ‘experimental design’ point of view. Atherinops affinis
lives longer, attains larger sizes and spawns repeatedly
(iteroparity), more so than M. menidia. Species-specific
life-history differences may have contributed to the observed
differences in CnGV patterns.
(c) Implications for a changing climate
We posit that CnGV will be the principal mechanism by
which ectotherms adapt to temporal gradients such as
those elicited by global climate change. If so, our findings
indicate that even small increases in mean temperature
will alter local genotype frequencies in many species.
Within species ranges, phenotypic similarity rather than
divergence is expected owing to the opposing effects of
genetic and plastic responses. In silversides, for example,
some sub-maximal growth capacity presently confers the
highest fitness at a given latitude. A rise in temperature
would result in ‘too fast’ growth of the previously fittest
genotypes, meaning that they will incur higher physiological growth costs than previously less-successful slower
growing genotypes, which then will become the fittest at
this location. The overall effect is a poleward migration
of genotypes, either literally (if possible) or via natural
selection, which remains masked by plastic responses to
temperature. Empirical evidence for such temporal
CnGV is still sparse but increasingly emerging [44 – 47].
Genetic shifts may produce little phenotypic change
within a species range [6], but at its extremes climate
change will have visible consequences. Species ranges
should gradually shift towards higher latitudes, because
at low latitudes, the genetic potential to evolve lower
growth capacities in response to higher temperatures is
exhausted, and habitat will be lost. At high latitudes,
new habitat will become available to the most extreme
genotypes, i.e. those with the highest species-specific
growth capacities. This prediction is consistent with the
already large and expanding evidence for shifting distributions in many marine and terrestrial taxa worldwide
(e.g. [48 – 50]). In addition, the predicted increases in
poleward heat transport [1] entail that warming will
likely be disproportional at higher than lower latitudes,
thus altering seasonality gradients and implying poleward
expansions rather than uniform shifts of species ranges.
We are grateful to the many persons who helped during field
sampling: Elizabeth Brown, Greg Callier, Jorge A. Rosales
Casián, Jeff Crooks, Tara Duffy, Rikke Preisler, Gary
Vonderhohe and Kerstin Wasson. Bill Chamberlain and
Steve Abrams greatly facilitated our experiments at Flax
Pond Laboratory. Soojin Jeon and Annalyse Moskeland
helped with daily nauplii counts during the growth
efficiency trials, while Owen Doherty assisted in retrieving
temperature data from the Research Data Archive (RDA).
RDA is maintained by the Computational and Information
Systems Laboratory (CISL) at the National Center for
Atmospheric Research (NCAR). This study was funded by
a grant from the US National Science Foundation
(OCE0425830) to D.O.C.
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