Proximate causes of adaptive growth rates: growth efficiency variation among latitudinal populations of Rana temporaria

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1 doi:1.1111/j x Proximate causes of adaptive growth rates: growth efficiency variation among latitudinal populations of Rana temporaria B. LINDGREN & A. LAURILA Population Biology/Department of Ecology and Evolution, Evolutionary Biology Center, Uppsala University, Uppsala, Sweden Keywords: countergradient variation; food consumption; growth; growth efficiency; gut length; latitudinal variation; phenotypic plasticity; Rana temporaria; tadpole. Abstract In ectothermic organisms, declining season length and lower temperature towards higher latitudes often select for latitudinal variation in growth and development. However, the energetic mechanisms underlying this adaptive variation are largely unknown. We investigated growth, food intake and growth efficiency of Rana temporaria tadpoles from eight populations along a 15 km latitudinal gradient across Sweden. To gain an insight into the mechanisms of adaptation at organ level, we also examined variation in tadpole gut length. The tadpoles were raised at two temperatures (16 and 2 C) in a laboratory common garden experiment. We found increased growth rate towards higher latitudes, regardless of temperature treatment. This increase in growth was not because of a higher food intake rate, but populations from higher latitudes had higher growth efficiency, i.e. they were more efficient at converting ingested food into body mass. Low temperature reduced growth efficiency most strongly in southern populations. Relative gut length increased with latitude, and tadpoles at low temperature tended to have longer guts. However, variation in gut length was not the sole adaptive explanation for increased growth efficiency as latitude and body length still explained significant amounts of variation in growth efficiency. Hence, additional energetic adaptations are probably involved in growth efficiency variation along the latitudinal gradient. Introduction Environmental stress is an important selective factor shaping intraspecific variation in life histories. A classic example of environmental stress is large scale climatic variation along latitudinal and altitudinal gradients selecting for clines in body size, growth and development (Endler, 1977; Conover & Schultz, 1995; Arendt, 1997; Hoffmann et al., 23). For example, increased growth and development rates towards higher latitudes have been found in a number of ectotherm species ranging from invertebrates to fish (Levins, 1969; Berven et al., 1979; Berven & Gill, 1983; Conover & Present, 199; Blanckenhorn & Fairbairn, 1995; Conover et al., 1997; Arnett & Gotelli, 1999; Imsland et al., 2; Jonassen et al., 2; Gilchrist et al., 21; Palo et al., 23). This Correspondence: Anssi Laurila, Population Biology/Department of Ecology and Evolution, Evolutionary Biology Center, Uppsala University, Norbyvägen 18D, SE Uppsala, Sweden. Tel.: ; fax: ; anssi.laurila@ebc.uu.se variation is adaptive as it ensures the completion of development and growth under harsh environmental conditions. Although latitudinal variation in growth rate has been repeatedly established, the physiological mechanisms underlying the latitudinal growth rate variation are not well understood (Garland & Adolph, 1991; Spicer & Gaston, 1999). Adaptive variation in growth efficiency, the capacity to convert ingested energy into biomass, is one potential mechanism for increased growth performance. Most of the studies focusing on variation in growth efficiency have been conducted in teleost fishes. These studies have found that in order to maintain high growth rate, high latitude populations may consume more food, have a higher capacity to convert, or use both these means (Present & Conover, 1992; Billerbeck et al., 2; Imsland et al., 2; Jonassen et al., 2). The only study on growth efficiency we are aware of in other animal groups is a study on Drosophila melanogaster, in which flies originating from high latitude populations had higher growth efficiency than those from low 82

2 Proximate causes of adaptive growth rates 821 latitudes (Robinson & Partridge, 21). The anatomical and physiological adaptations behind this variation remain enigmatic. A possible explanation for variation in growth capacity and efficiency can be found in the theory of optimal digestion (Sibly, 1981), whereby an increased gut length should promote more efficient digestion and hence have a positive effect on growth (Sibly, 1981; Relyea & Auld, 24). However, although gut length, like the size of many other organs, is a plastic trait (Piersma & Lindström, 1997; Piersma & Drent, 23; Relyea & Auld, 24), there appear to be no comparative studies on gut length conducted with multiple populations under common garden conditions. Is adaptation to temperature or growth season variation behind the geographical variation in growth along climatic gradients? Since mean ambient temperatures typically decrease as latitude increases, it is expected that high latitude populations would perform better than low latitude populations at lower temperatures, whereas the opposite would be true at higher temperatures (Levinton & Monahan, 1983; Lonsdale & Levinton, 1985). However, if variation is because of adaptation permitting the northern individuals to increase their rate of growth and development in response to more stringent time constraints in higher latitudes, high latitude populations should perform better than low latitude populations regardless of temperature (Conover & Schultz, 1995; Yamahira & Conover, 22). For example, Laugen et al. (23a) showed that the latitudinal cline in development rate in the common frog (Rana temporaria) larvae was not correlated with mean ambient temperatures across latitude, but strongly correlated with growth season length, suggesting that season length is a more important selective force than temperature. The aim of this study was to investigate the mechanisms underlying the latitudinal variation of growth rates in R. temporaria tadpoles. R. temporaria is the most widespread amphibian in Europe (Fog et al., 1997) and provides an excellent system to study latitudinal variation. Previous studies with Scandinavian R. temporaria populations have found increasing larval growth and development rates towards higher latitudes (Merilä et al., 2; Laurila et al., 21; Laugen et al., 23a; Palo et al., 23). We collected R. temporaria embryos from eight populations along the latitudinal gradient across Sweden, and measured growth, food intake, growth efficiency and gut length in tadpoles raised under common garden conditions in the laboratory. We addressed the following questions. First, do R. temporaria populations along the latitudinal gradient differ in food intake and growth efficiency, and which trait better explains variation in growth rate? Secondly, do R. temporaria populations differ in gut length and does variation in gut length explain variation in growth performance? Thirdly, how does temperature affect food consumption, growth efficiency and gut length, and do low and high latitude populations differ in their responses? Methods We collected freshly laid eggs of R. temporaria from seven to nine families in eight populations along a 15 km latitudinal gradient across Sweden (Fig. 1, Table 1). The eggs were transported to the laboratory in Uppsala, and c. 5 eggs per family were distributed evenly over three.9 L opaque plastic containers. The eggs were reared at 16 C until they had hatched and reached Gosner developmental stage 25 (absorption of gills, Gosner, 196). The water in each container was changed every 3 days. After reaching stage 25, the tadpoles were fed chopped spinach ad libitum. After 3 days (day of the experiment), 4 tadpoles were taken at random from each population (Table 1) and 2 tadpoles were placed in each of the two temperature treatments (16 and 2 C) arranged in two constant temperature rooms. Four to six tadpoles from each family were used and placed in equal numbers in the two treatments. Both treatments represent normal temperatures tadpoles encounter in their natural environment (J. Merilä, A. Laurila, D. Lesbarreres, A.T. Laugen & K. Räsänen, unpublished). The tadpoles were kept individually in.9 L opaque plastic containers and fed Spirulina algae discs (WardleyÒ, Secaucus, NJ, USA) ad libitum. The tadpoles were allowed to adjust to the new food and temperature regimes for eight days before any experimental recordings started. When quantifying food consumption, each Spirulina disc was weighed with an electronic balance (precision.1 mg) before being added to the container. After 3 days the remaining food Barsjön Kabusa Karesuando Uppsala Jukkasjärvi Mjösjö N Hamptjärn Söderfors 1 km Fig. 1 Map of Sweden showing the locations of the studied Rana temporaria populations.

3 822 B. LINDGREN AND A. LAURILA Table 1 Study populations, sampling dates, number of collected families and number of individuals used in analyses. Locality Sampling date No. of families No. of individuals 16 C 2 C Kabusa 55 4 April Barsjön 55 9 April Uppsala April Söderfors 6 35 April Mjösjö May Hamptjärn May Jukkasjärvi May Karesuando May was retrieved, dried at 6 C for 24 h, and weighed again in order to obtain an estimate of food consumption. This was repeated for three 3-day periods (i.e. days 9 12, and of the experiment). Water was changed in conjunction with feeding. We used a 1 : 9 mixture of carbon filtered tap water and deionised water, aerated for a minimum of 24 h before use, throughout the experiment. Photoperiod in the laboratory was 16 h light : 8 h dark. Wet weight of each tadpole was measured with an electronic balance at the beginning (day 9) and end (day 18) of the experiment. At the end of the experiment, the tadpoles were killed with an overdose of the anaesthetic MS-222 (methanesulfonate salt; Sigma-AldrichÒ, Steinheim, Germany) and stored in 7% alcohol for later measurements. The body length was measured using digital callipers (to the precision of.1 mm) and the development stage was determined according to Gosner (196). The gut was dissected out of each tadpole and its total length (GL) was measured with digital callipers. Calculation of growth efficiency The data on larval growth rate and food consumption were used to calculate daily growth rate, daily food consumption and gross growth efficiency. Mean daily growth rate (GR, g day )1 ) was estimated as: GR ¼ BW f BW i t where t is the time in days the experiment lasted; BW i is the initial body weight when the experiment started and BW f is the final body weight at the end of the experiment. Mean daily food consumption (FC, g day )1 ) was calculated as: FC ¼ F a F r t where F a is the weight of the added food and F r is the weight of the retrieved food. This allowed us to estimate the gross growth efficiency (GGE, %; e.g. Wootton, 199): GGE ¼ 1 GR FC indicating how efficiently the consumed food is used to increase body weight, i.e. the capacity to convert food into body mass. As Spirulina discs contain essentially no water, but growth increment was measured as wet mass, the obtained GGE values typically reach over 1%. Statistical analyses The total number of individuals in the final analyses was 313. There was no mortality during the experiment, but the sample size in the statistical analyses varied from 18 to 2 larvae per treatment combination because of errors during the measuring procedures. As the dataset included only two or three individuals from each family per treatment combination, including family effects in the models was not meaningful. Initial GLMs indicated that population and population temperature interactions were highly significant in all response variables. To gain more insight into the latitudinal variation the data were analysed with mixed model ANCOVAs using population term as a random factor and latitude as a covariate. We used REML estimation for random effects and Type III sums of squares for fixed effects as implemented in Proc Mixed in SAS V8 (Littell et al., 1996). In an additional set of analyses, we controlled for body size differences by including initial body weight, or body length and development stage (in gut length analyses) as covariates. Interactions between body size/development stage and temperature were not significant in any of the analyses (P >.5). Results Growth rate Growth rate (GR) increased with latitude and temperature with the two northernmost populations having the highest values (Table 2, Fig. 2). However, GR in the two southernmost populations did not differ from those of the two southern mid-latitude populations. The significant latitude treatment interaction indicated that the difference between the temperature treatments was smaller at higher latitudes resulting in a steeper increase of GR in low temperature (Table 2, Fig. 2a). Initial body weight had a significant positive effect on growth rate [b ¼.118 ±.2 (SE)], and the results remained largely unaffected after correcting for body weight differences (Table 2, Fig. 2b). The northernmost population had very high growth rate early in the experiment explaining the

4 Proximate causes of adaptive growth rates 823 Table 2 Mixed model ANOVA tables showing the effects of population origin, latitude and temperature regime on mean daily growth rate, food consumption and growth efficiency. Source of variation Random effects Variance (SE) Z Fixed effects d.f. F Growth rate Population.25 (.16) , ** Residual.97 (.8) 12.31*** Temperature 1, *** temperature 1, *** Population.13 (.8) , ** Residual.67 (.5) 12.29*** Temperature 1, *** temperature 1, *** Initial body weight 1, *** Food consumption Population 1, 6.1. Residual.44 () Temperature 1, *** temperature 1, ** Population.5 () 1, Residual.19 () Temperature 1, *** temperature 1, *** Initial body weight 1, *** Growth efficiency Population (754.2) , ** Residual (277.69) 12.31*** Temperature 1, *** temperature 1, *** P <.1;*P <.5; **P <.1; ***P <.1. drop of relative growth estimates after inclusion of body weight in the model (Fig. 2). Food consumption Food consumption was higher at high temperature (Table 2, Fig. 3). Although an initial analysis of the mean daily food consumption showed significant differences between populations (F 7,297 ¼ 15.68, P <.1), mixed model found no significant latitude main effect (Table 2). However, a significant latitude temperature interaction indicated that, although there was no effect of latitude at high temperature, the two northern populations consumed more food at low temperature bringing about a positive latitude effect. Large tadpoles had higher food consumption (Table 2, b ¼.39 ±.2), and when initial body weight was included in the model latitude had a negative effect on food consumption. This was especially the case at high temperature as indicated by the significant latitude temperature interaction (Table 2, Fig. 3b). Gross growth efficiency Gross growth efficiency was significantly affected by latitude and temperature (Table 2, Fig. 4). In general, GGE was higher at high temperature and in the northern populations. However, there was no difference between the two southernmost and the two southern mid-latitude populations (Fig. 4). At low temperature the highest GGEs were found in the two northernmost populations. At high temperature, one of the northernmost populations still had the highest GGE, but was followed by the two northern mid-latitude populations rather than the other northern population (Fig. 4). The significant latitude treatment interaction indicated that the difference between the temperature treatments was smaller at higher latitudes resulting in steeper increase of GGE at low temperature (Table 2, Fig. 4). GGE was not affected by initial body weight (F 1,31 ¼.93, n.s.). Gut length Gut length (GL) was longer at high temperature and increased with latitude (Table 3, Fig. 5a). The increase in GL with latitude was much more profound in the lower temperature treatment causing the significant latitude temperature interaction (Table 3, Fig. 5a). After controlling for body length and development stage, latitude had a significant influence on GL, but temperature treatment was no longer significant (Table 3). Both body length (b ¼ ± 1.6) and development stage (b ¼ 3.3 ± 1.3) had significant positive effects on GL with larger and more developed tadpoles having longer guts (Table 3). However, when body length and development stage were taken in account the relative GL was larger in low than in high temperature treatment (Fig. 5b). Again, the significant latitude temperature interaction indicates much steeper increase in relative GL with latitude at low temperature treatment (Table 3, Fig. 5b). To get an insight into how well variation in GL explains variation in GGE, we repeated the analyses of GGE by including both GL and body length in the model as covariates. We found that although GL (b ¼.59 ±.21) and body length (b ¼ ± 4.3) both had significant positive effects on GGE, latitude, temperature and their interaction all still had strong,

5 824 B. LINDGREN AND A. LAURILA (a).7 Mean daily growth rate (g day 1 ) (b).7 Mean daily growth rate (g day 1 ) Fig. 2 Mean daily growth rate (least square mean ± SE) in relation to latitude of origin. (a) Without initial body weight and (b) with initial body weight included in the statistical model. Squares: tadpoles raised at 16 C, circles: tadpoles raised at 2 C. (a).18 Mean daily food consumption (g day 1 ) Mean daily food consumption (g day 1 ) (b) Fig. 3 Mean daily food consumption (least square mean ± SE) in relation to latitude of origin. (a) Without initial body weight and (b) with initial body weight included in the statistical model. Squares: tadpoles raised at 16 C, circles: tadpoles raised at 2 C. independent effects (Table 4). This result suggests that although variation in GL contributes to the increased GGE at higher latitudes, it is not the sole adaptive mechanism. Discussion In accordance with previous studies on R. temporaria (e.g. Laurila et al., 21; Laugen et al., 22; Palo et al., 23), we found increased growth rates towards higher latitudes. Furthermore, we found increased growth efficiency towards higher latitudes, whereas food consumption showed little latitudinal variation. These results suggest that increased growth efficiency in high latitude populations is one of the main physiological mechanisms behind the latitudinal growth rate variation in R. temporaria, which is well in accordance with the few previous ectotherm studies on growth rates conducted along latitudinal gradients (Present & Conover, 1992; Imsland et al., 2; Jonassen et al., 2; Robinson & Partridge, 21). Hence, increased growth efficiency appears to be a general mechanism by which high latitude populations ensure high growth rates under temperature stress or time constraints. Temperature had a strong effect on both growth and growth efficiency. Although the northernmost populations generally outperformed the southern ones in both treatments, the latitudinal patterns in growth and growth efficiency were stronger at low temperature. This suggests that the northern populations are even better adapted to maintain high growth rates in low temperature. This result cannot be explained in terms of latitudinal temperature variation as highest mean ambient temperatures across the whole larval period are found in the northern mid-latitudes (Laugen et al.,

6 Proximate causes of adaptive growth rates 825 Gross growth efficiency (%) Fig. 4 Mean gross growth efficiency (least square mean ± SE) in relation to latitude of origin. Squares: tadpoles raised at 16 C, circles: tadpoles raised at 2 C. 23a), and the southern populations actually meet the lowest temperatures along the gradient during embryonic and early larval development (Ståhlberg et al., 21; Laugen et al., 23b). Hence, these results lend little support to the temperature adaptation hypothesis (Levinton & Monahan, 1983; Lonsdale & Levinton, 1985, see also Hoffmann et al., 23; Sørensen et al., 25 for temperature extremes), but instead suggest that latitudinal growth variation has mainly evolved in response to the more stringent time constraints (Conover & Schultz, 1995; Laugen et al., 23a). However, another possible explanation for the frequent temperature latitude interactions is that the fast-growing and -developing northern populations had already passed the period of fastest growth in high temperature leading to relatively low estimates in this treatment. This is especially the case in the northernmost population, which showed very high growth early in the experiment. In the future, such ontogenetic factors should be taken into account. For example, studies following growth dynamics over the whole larval period would be interesting in that they might elucidate the extent of ontogenetic variation in growth performance along climatic gradients. As a potential anatomical explanation for increased growth efficiency we examined tadpole gut length. We found both latitudinal and temperature effects as gut length increased with latitude especially in low temperature. After controlling for body size, the relative gut length was larger in the low temperature in all the populations except in the most southern one. These results support the idea that a longer gut is more efficient at digesting (Sibly, 1981), and add to the evidence that gut size is a plastic trait that may respond rapidly to environmental variation (Piersma & Drent, 23). For example, previous studies on tadpoles have found that tadpoles respond to competitors with increased gut length, whereas presence of a predator induces a shorter gut (Relyea & Auld, 24). We found relatively longer guts in the low temperature in all the populations except the two southernmost ones. This indicates temperature-induced adaptive plasticity in gut length in tadpoles and suggests that the high growth efficiencies found in the low temperature are partly due to increased gut length. However, even after controlling for variation in body size and gut length, we found a significant relationship between latitude and growth efficiency, indicating that variation in gut length is not the only mechanism behind increased growth efficiency in high latitudes. It seems possible that part of the variation in growth efficiency among populations may be explained by variation at protein level. One possible candidate is isozyme variation in digestive enzymes, which has been found to affect food utilization efficiency in fish (Rungruangsak-Torrissen et al., 1999). Although we found differences in food consumption among the populations, no clear latitudinal trend in this trait could be established. Indeed, there was evidence that food consumption increased towards higher latitude at low temperature, but decreased at high temperature. However, after correcting for body size, there was a nonsignificant negative relationship between food consumption and latitude, and this was more evident at high temperature. This suggests that the northern tadpoles tend to ingest less food for a given body size. The lack of a clear latitudinal pattern in consumption is in accordance with some previous studies on fish (Imsland et al., 2; Jonassen et al., 2). However, in the Atlantic silverside (Menidia menidia) high latitude populations had increased consumption rates (Present & Conover, 1992; Billerbeck Table 3 Mixed model ANOVA tables showing the effects of population origin, latitude, temperature regime body length and development stage on gut length. Random effects Variance (SE) Z Fixed effects d.f. F Population (166.32) 1.66* 1, * Residual (39.41) 12.29*** Temperature 1, *** temperature 1, *** Population (14.24) , * Residual (16.17) 12.23*** Temperature 1, temperature 1, * Body length 1, *** Development stage 1, ** P <.1; *P <.5; **P <.1; ***P <.1.

7 826 B. LINDGREN AND A. LAURILA (a) 16 Gut length (mm) (b) 16 Gut length (mm) Fig. 5 Mean gut length (least square mean ± SE) in relation to latitude of origin. (a) Without initial body weight and (b) with initial body weight included in the statistical model. Squares: tadpoles raised at 16 C, circles: tadpoles raised at 2 C. et al., 2). The significant variation in food consumption among R. temporaria populations found in this study suggests that the selective pressures faced by foraging tadpoles may vary among the populations. High foraging activity is costly in terms of increased predation risk (Anholt & Werner, 1995), and it seems possible that variation in food consumption reflects differences in predation risk in the source ponds. However, the costs of low foraging activity (and hence lower growth) are likely to be higher in the more time-limited northern populations, which may partly explain the higher growth efficiency in the north. Although we found significant differentiation in all studied traits, there was often considerable variation around the latitudinal trend in tadpole traits, suggesting that other selective factors than large-scale climatic variation may also have acted upon these traits. This is expected as there is increasing evidence that local selective factors (e.g. temperature, pond desiccation risk, predation) can create significant local variation in growth and development (Relyea, 22; Skelly, 24; see also discussion on food consumption above). For example, the fact that the two southern populations appear to deviate from the latitudinal trend in many analyses can possibly be explained by the fact that both these populations are late breeders, probably because these ponds take longer to reach suitable breeding temperature in early spring. This may lead to a shorter season length than in the other populations from the same latitude and explain their relatively high growth rates. As the experiment was conducted with field-collected animals, the differences among the populations can be due to genetic or environmental maternal effects. Although environmental maternal effects can be important in creating population differentiation, earlier quantitative genetic studies have found much weaker maternal than additive genetic effects on larval life history traits both within and between Scandinavian R. temporaria populations (Laugen et al., 22; Laurila et al., 22). However, caution is needed in interpreting the present results as other studies have found strong maternal effects on growth of R. temporaria (Sommer & Pearman, 23). Furthermore, very little appears to be known about heritability of growth efficiency in ectotherms (but see Thodesen et al., 21). In conclusion, we have showed that latitudinal variation growth rate in R. temporaria tadpoles can largely be explained in terms of increased growth efficiency towards higher latitudes. The increase in growth efficiency was partly explained by a relatively longer (and more efficient) digestive tract in high latitude populations. Both growth and growth efficiency Table 4 Mixed model ANOVA tables showing the effects of population origin, latitude, temperature regime, body length and gut length on growth efficiency. Random effects Variance (SE) Z Fixed effects d.f. F Population (529.28) 1.6 1, ** Residual (222.8) 12.25*** Temperature 1, *** temperature 1, *** Body length 1, ** Gut length 1, ** P <.1; *P <.5; **P <.1; ***P <.1.

8 Proximate causes of adaptive growth rates 827 were higher in the north irrespective of temperature, suggesting that adaptation has occurred to maximize growth during the short growing season. Gut length was significantly longer in low temperature in most of the populations, indicating significant plasticity in organ size. Studies on isozyme and activity variation of digestive enzymes are likely to prove fruitful in gaining further understanding of the evolution of growth efficiency variation along geographical gradients. Acknowledgments We thank Annika Lydänge and Simon Kärvemo for help in the laboratory, and Wolf Blanckenhorn, Gerard Malsher and Céline Teplitsky for comments on earlier versions of this manuscript. This work was funded by the Swedish Research Council (to AL) and the Zoological Foundation (BL). The experiment was carried out with the permission of the Ethical Committee for Animal Experiments in Uppsala County. 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