Interpreting Geographic Variation in Life-History Traits 1

Transcription

1 AMER. ZOOL., 23:8597 (1983) Interpreting Geographic Variation in LifeHistory Traits 1 KEITH A. BERVEN AND DOUGLAS E. GILL Department of Zoology, University of Maryland, College Park, Maryland SYNOPSIS. The geographic variation in the length of the larval period and the size at metamorphosis of the wood frog, Rana sylvatica, is examined for populations in the tundra of Canada, the mountains of Virginia, and the lowlands of Maryland. We argue that the observed differences in developmental plasticity, heriisbilities and genetic covariances of traits among localities result from differential selection pressures in each environment, and are related to the physiological constraints inherent in development and to the degree of compromise between the timing and size at metamorphosis allowed in each environment. In Maryland populations fitness has been maximized by evolutionary changes in size alone; body size in this population is canalized, has low heritability and is highly correlated with juvenile survival relative to developmental time. In Canada, minimum developmental time yields maximum fitness; the length of the larval period in this population is canalized and genetically monomorphic relative to body size. In contrast, fitness in the Virginia populations has been determined by correlated and pleiotropic effects of genes on both developmental time and larval body size, and both traits are equally canalized, affect juvenile survivorship equally and display moderate heritabilities. These results stress the importance of interpreting variation in lifehistory traits relative to constraints inherent in development and those imposed by the environment. Heritability and survivorship data support the general notion that fitness traits should have low levels of additive genetic variation, but also suggest that antagonistic pleiotropy may act to preserve genetic variation in fitness traits under simultaneous selection, and caution against inferring evolutionary importance of individual traits without considering the possible presence of pleiotropy. INTRODUCTION A major contention of lifehistory theory is that the traits that compose an organism's life history are "coadapted and designed by natural selection to solve a particular ecological problem" (Stearns, 1976). The implication of this theory is that lifehistory traits have a genetic basis and have coevolved under the influence of demographic selection. However, based on recent considerations of developmental and morphological constraints and physiology, Stearns (1980) has challenged the assumption that lifehistory traits are unrestricted entities that are free to covary in response to selection. He also questions the use of quantitative genetics to infer coadaptation of lifehistory traits and argues that meaningful interpretations of lifehistory evolution should also include aspects of whole organism ontogeny and developmental 1 From the Symposium on The Interface of LifeHistory Evolution, WholeOrganism Ontogeny and Quantitative Genetics presented at the Annual Meeting of the American Society of Zoologists, 2730 December 1981, at Dallas, Texas. 85 ecology. Indeed one goal of this symposium will be to seek a common boundary between 1) whole organism ontogeny, which focuses on developmental constraints, plasticity and canalization and 2) quantitative genetics which focuses on changes in heritabilities, covariances and correlations, to gain a better understanding of how lifehistory tactics may evolve. Amphibian larval development provides an excellent case to examine this interface. The underlying physiological mechanisms controlling metamorphosis are well understood (Kollros, 1961; Etkin, 1963, 1968), much ecological literature demonstrates the effects of abiotic and biotic factors on metamorphic patterns (see review by Wilbur, 1980), genetic parameters can be quantified (Travis, 1981; Berven, 1981a) and ecological studies can directly relate changes in larval patterns to survival and reproductive success. In this paper we summarize a large body of information about the larval period of a single species, the wood frog, Rana sylvatica, to examine the interface between ontogeny and quantitative genetics. We Downloaded from by guest on 15 October 2018

2 86 K. A. BERVEN AND D. E. GILL focus on aspects of geographic variation in larval patterns among three populations. The first is a midlatitude (38 N), lowelevation (42 m), population in Maryland, the second a midlatitude (38 N), highelevation (1,200 m), population in the Shenandoah Mountains of Virginia, and the third, a highlatitude (59 N), lowelevation (50 m), population in the tundra near Churchill, Manitoba, Canada. These localities represent three ecologically different environments near the extreme northern and southern limits of the wood frog's range, and near the maximum elevation at which this species is found. We begin with a brief summary of the ecology of this species. We then 1) document the geographic variation in larval developmental patterns (both genetic and environmental components), 2) examine the phenotypic plasticity of larval traits, 3) characterize the nature of the genetic variation underlying the phenotypic variation within each population (heritabilities and genetic covariances) and 4) document that larval traits are indeed important to fitness and responsive to selection. After relating correlated and antagonistic aspects of larval development, degree of canalization and changes in genetic structure, to differences in selection pressures and geographic variation in larval patterns, we shall conclude by discussing the implications of this study to lifehistory evolution in general. THE GEOGRAPHICAL ECOLOGY OF RANA SYLVATICA Wood frogs are widely distributed throughout North America, ranging from the mesic forests of the southern Appalachians in Tennessee and northern Georgia to the tundra within the Arctic Circle. The life cycle includes an aquatic stage followed by a terrestrial juvenile and adult period. This pattern varies considerably throughout their geographical distribution (Martof and Humphries, 1959; Berven, 1982a, b). The frogs typically breed in small temporary ponds during the first warm rains of spring, often before the ponds are free of ice. Eggs are deposited in early February in the southern part of their range, but not until late June in the extreme northern localities (Martof and Humphries, 1959; Kessel, 1965; Berven, 1982a). The duration of the larval period varies geographically, but metamorphosis usually occurs before the first winter. However, at the northern limits of their range larvae may be forced to overwinter (Hildebrand, 1949), and it is not known whether they can successfully complete metamorphosis the following year. Following metamorphosis, individuals mature in neighboring forests. Males mature at 13 yr and females at 24 yr, depending on locality (Bellis, 1961; Collins, 1975; Berven, 19826). Adult body size and the size and number of eggs produced by females also varies geographically (Martof and Humphries, 1959; Nagel and Meeks, 1973; Berven, 1982ft). GEOGRAPHICAL VARIATION IN LARVAL TRAITS Larval developmental patterns vary considerably both within and among localities throughout their geographic range. In general, larval periods are shortest in the north (Alaska: 4678 days [Herreid and Kinney, 1967]; Massachusetts: 58 days [Hinckley, 1885]) and increase in duration to the south (Maryland: 7392 days [Berven, 1982a]; Tennessee: 84 days [Meeks and Nagel, 1973]) and with elevation (Virginia: days [Berven, 1982a]). Larval body size increases clinally with both latitude (Maryland: g [Berven, 1982a]; Minnesota: g [Fishbeck, 1968]; Alaska: g [Herreid and Kinney, 1967]) and elevation (Virginia: g[berven, 1982a]). Although these data document geographic variation in larval developmental patterns, they say nothing about the degree to which the observed variation represents genetic differentiation versus phenotypic plasticity. A detailed analysis aimed at identifying the environmental and genetic contributions to the interelevation differences in larval patterns between Maryland and Virginia populations has previously been reported (Berven, 1982a). In that study, reciprocal field transplant experiments of larvae between elevations demonstrated that environmental differences (particu Downloaded from by guest on 15 October 2018

3 GEOGRAPHIC VARIATION IN LIFEHISTORY TRAITS 87 larly temperature) between the two localities accounted for most (7388%) of the observed phenotypic variation. However, a significant portion of the observed variation in larval traits between populations was preserved regardless of the environment in which the larvae developed. Similar results were obtained when larvae from both localities were raised in the laboratory at a constant density at each of six temperatures (Berven, 1982a). An analysis of covariance treating temperature as the covariate revealed that larvae of mountain origin had significantly shorter larval periods and were larger at metamorphic climax than larvae of lowland origin at all temperatures. That these observed differences represented true genetic differences and not nongenetic maternal effects was partially confirmed by the results of a set of reciprocal crosses between males and females of mountain and lowland origin (Berven, 1982a). That study revealed that the shorter larval periods of mountain larvae were due entirely to the larger egg size of mountain females. Egg size also influenced larval body size but a significant portion of the variation in body size was also attributed to genetic differences between the two populations. More recently, larvae derived from Canadian populations, near Churchill, Manitoba, have been reared in the laboratory under conditions identical to those previously used and their larval developmental patterns can now be compared to larvae of Maryland and Virginia origin (Fig. 1). In contrast to Maryland and Virginia larvae, Canadian larvae were far less sensitive (lower slopes) to temperature effects on both larval period lengths and larval body size at metamophosis (an analysis of covariance to test for homogeneity of slopes among the three populations: Larval differentiation rates; F (2> io7) = 23.1, P < 0.001; larval body size; F (5U26) = 4.6, P < 0.025) (Fig. 1). As a consequence, particularly at low temperatures, Canadian larvae had significantly shorter larval periods and metamorphosed at a significantly smaller size than those from either Maryland or Virginia. Because these values were A. B _ X z 0 1. D y yo Y M... y = / f = 0 97 v y* K Lowland y = 2.68x5 19 r = 0.96 ^ r i f T undr a y 197 «d 2 I r : Tcmoeratuie ( C ) Fic. 1. Temperature dependence of (A) differentiation rates and (B) size at metamorphic climax of lowland (Maryland; closed symbols), mountain (Virginia; open symbols) and tundra (Manitoba; stars) wood frogs. Each symbol equals the mean of three replicate pans of eight larvae per pan from 3 mountain, 3 lowland and 5 tundra ponds. determined from fullsib crosses it is not possible to isolate the nongenetic maternal effects; however, egg sizes from tundra populations were considerably smaller (X = 1.6 mm) than eggs of mountain origin (X = 2.25 mm) and somewhat smaller than eggs of lowland origin (X = 1.83 mm). Thus, although the smaller larval size may include nongenetic maternal effects, egg size differences cannot be invoked to explain the faster developmental rates. In summary, environmental differences among localities account for a major portion of the observed variation in larval patterns. Nevertheless, a significant portion of the observed variation in larval period Downloaded from by guest on 15 October 2018

4 88 K. A. BERVEN AND D. E. GILL LOWLANDS (Maryland) A. D.n.ity (par 2 IllartO Damlty (par a IU*f*) Dantlty (par 2 IIUr») FIG. 2. The effect of temperature and density on the (A) length of the larval period and (B) size at metamorphosis of larvae derived from Maryland, Virginia and Manitoba populations. Mean ± 1 SE of three replicate crosses are shown. length and larval body size among these populations has a genetic basis. DEVELOPMENTAL PLASTICITY OF LARVAL TRAITS Besides temperature, density has long been recognized as a factor generating large phenotypic differences among larval wood frogs (Adolph, 1931). Both field and lab studies have shown that increasing larval densities prolong the larval period, reduce metamorphic size, and more importantly, reduce the probability of successful metamorphosis (Herreid and Kinney, 1967; Wilbur, 1976, 1977; SmithGill and Gill, 1978). Although the relative importance of temperature and density has never been measured, it is generally thought that because temperature differences among ponds within a particular locality are likely to be small relative to amonglocality variation (i.e., latitudinal or elevational), it is reasoned that variation in conspecific density is probably the critical factor contributing to amongpond, withinlocality phenotypic variation in developmental patterns. However, the relative plasticity of developmental rates or body size has never been examined nor has the degree to which plasticity of larval traits differs between populations been investigated. To compare the responses of larvae Downloaded from by guest on 15 October 2018

5 89 GEOGRAPHIC VARIATION IN LIFEHISTORY TRAITS TABLE 1. A four factor ANOVA (SAS) of the effects of population (Manitoba, Maryland and Virginia), temperature and density on (A) length of larval period and (B) size of metamorphic climax.* Source ,377 1,536 (B) MS * * * * * * * * * * * * * * Coefficients of determination 0.54(0.27) 0.13(0.14) ' Significant effects (P < 0.05). derived from different populations to variation in larval densities, larvae from Maryland, Virginia and Canada were raised in the laboratory at densities ranging from a single individual per pan (2 liters of water) to 32 individuals per pan at each of three temperatures (15, 18, 22 C). For each larva the size (volume of water displaced in a graduated cylinder) and date of metamorphosis (TaylorKollros stage XX) was determined. This experiment (Fig. 2) revealed large and significant (Table 1) differences in developmental time and body size among larvae raised at different temperatures and densities, and among larvae derived from different populations. Temperature had the greatest impact and accounted for most of the observed variation (Table 1). In addition, there were several significant interactions (Table 1). Of particular interest to the present study is the population X density interaction. The nature of the population X density interaction was evaluated for each trait by comparing the relative sensitivities of each population to the variation in larval densities using techniques described by Zuber and Gale (1976). The general effect of each density treatment was first evaluated as the mean of all three populations for each density treatment within each temperature treatment (referred to as the environmental value). The mean larval period and mean body size for each population was then plotted against the corresponding environmental value (mean) for each density treatment. The slope of these regression lines measured the environmental sensitivity of each population, and differences in these slopes among the populations reflect differences in their relative sensitivities. An analysis of covariance was used to test for equality of slopes and a posteriori tests for specific differences among the regression coefficients of each population were tested using the Simultaneous Test Procedure (STP) at the 5% level of significance. These comparisons (shown graphically for 18 C in Fig. 3 and for all temperatures in Table 2) revealed striking differences in the responses of the three populations to variation in larval densities. The regression coefficients for developmental time of tundra larvae were significantly smaller at all temperatures than the regression coefficients of lowland larvae (Table 2A). This reflected the relatively small differences in the developmental times of tundra larvae among density treatments compared to the comparatively large differences in developmental times of lowland larvae for the same density treatments (Fig. 2). The slopes of mountain larvae were intermediate to Downloaded from by guest on 15 October 2018 Population Temperature Density Replicate Pop X temp Pop X density Pop X rep Temp X density Temp X rep Density X rep Pop X temp X density Pop X temp X rep Pop X density X rep Temp X density X rep Pop X temp X density X rep Error Total (A) MS

6 90 K. A. BERVEN AND D. E. GILL 18 C A LARVAL PERIOD LENGTH B. METAMORPHIC BODY SIZE / f /LOWLANDS R=.98 MOUNTAINS / y R=.9 1 / /,» ^ttf TUNORA y^^ R= Environmental Value (days) A / y o /f //.6.8 TUNDRA / R=92 MOUNTAINS H=.84 LOWLANDS R=.7 7 Environmental Value (ml) FIG. 3. Developmental sensitivity of (A) length of larval period and (B) size at metamorphic climax of lowland, mountain and tundra larvae to density treatments at 18 C. Each point represents the mean of 3 replicates. Regression coefficients and correlation coefficients are given for each population. See text for details. both tundra and lowland larvae; however, in most cases they did not differ significantly from the larvae of Canadian origin (Table 2A). In contrast, the pattern was reversed for metamorphic body size. The slopes for metamorphic body size of lowland larvae were smaller than those of tundra larvae, reflecting the relatively smaller variation in body size of lowland larvae among density treatments compared to the tundra larvae (Fig. 3, Table 2B). The slopes of mountain larvae were again intermediate, but did not differ significantly from the lowland larvae (Table 2B). The differential response of each population to variation in larval density can also be evaluated by comparing the coefficients for developmental time and larval body size within each population. For lowland and tundra larvae the regression coefficients for size and developmental time differ greatly (Table 2A, B) while in contrast, the regression coefficients for size and developmental time of mountain larvae are very similar. In summary, larvae derived from these three populations differed in their relative plasticity for developmental time and body size, and responded to the density treatments in three contrasting ways. Lowland larvae from Maryland responded with variable ages but constant size at metamorphosis. Tundra larvae from Manitoba responded with constant age but variable size, while mountain larvae from Virginia were intermediate with less sensitivity to density for both size and developmental time. NATURE OF THE GENETIC VARIATION UNDERLYING PHENOTYPIC VARIATION WITHIN POPULATIONS Evolutionary change in response to natural selection requires that phenotypic variation be heritable and there must be differential fitness according to the phenotype (Lewontin, 1974). Two important.61 Downloaded from by guest on 15 October 2018

7 GEOGRAPHIC VARIATION IN LIFEHISTORY TRAITS 91 variables from classical quantitative genetics bear on the evolutionary dynamics of variation in polygenic traits. These are the heritability of the trait and the genetic covariance between traits (Falconer, 1960). I have previously reported the results of a traditional halfsib analysis used to estimate the heritabilities and genetic covariances of larval traits from Maryland and Virginia populations (for details of experimental design see Berven, 1981a). In brief, developmental time in both populations was moderately heritable (lowland: 0.27 ± 0.07; mountains: 0.34 ± 0.10). In contrast, larval body size among mountain larvae was highly heritable (0.58 ± 0.17) compared to the insignificant heritability of body size in lowland larvae (0.08 ± 0.004). Phenotypic correlations between developmental rate and larval body size were negative in both populations (lowland: r p = 0.42; mountains: r p = 0.26). Thus in both populations slower developing larvae tended to metamorphose at a larger size than faster developing larvae. However, genetic correlations (based solely on the covariance of traits between males) differed strikingly between the two populations. Lowland populations had a positive genetic correlation (r A = ± 0.05) while mountain populations had a negative genetic correlation (r A = 0.86 ± 0.06). A similar halfsib analysis has not yet been done on Canadian populations. However, a preliminary analysis of five fullsib crosses has been made. Heritability estimates for fullsib crosses can be made from the ratio of the amongcross component of variation to the total variation. However, since such estimates will include a portion of the dominance variance, they must be taken as upper bounds. For developmental rate there were no significant amongcross differences (F (4,io2) = 1.79, NS) and heritability of developmental rate was very low (0.07 ± 0.02) and not significant. There were however, significant differences in metamorphic body size among fullsib crosses (F ( 4.io2) = 4.34, P < 0.003) and the heritability estimate was moderate (0.27 ± 0.05). The phenotypic correlation between TABLE 2. Comparisons of the developmental sensitivity of (A) larval period length and (B) metamorphic size o/rana sylvatica from three populations raised at three temperatures. * Tempera Results of ture CQ Lowland Mountains Tundra ANCOVA (A) Length of larval period F (2, 8) = 50.1 P < O F (2. 47) = 44.4 P < F(2.48) = 5.83 P < 0.01 (B) Size at metamorphic climax F(2,4 8, = 4.76 P < O.025 F (2, 47) = 8.93 P < O.001 F (248) = 6.02 P < 0.01 * Regression coefficients shown are derived from the density experiment shown in Figure 2. All regressions were significant (P < 0.05). See text for details of how they were calculated. Analysis of covariance (ANCOVA) tested for the homogeneity of slopes. Those slopes which did not differ at the 5% level (using STP) are underlined. developmental rate and body size was negative (r p = 0.21) and the genetic correlation was very low (r A = ± 0.14) and did not differ from zero. In summary, heritable variation in larval traits within populations does exist. However, the levels of additive genetic variance and the nature of the genetic correlations between traits differed dramatically among the three populations and suggest that selection may be operating differently in each environment. LARVAL TRAITS AS COMPONENTS OF FITNESS Because some to the observed phenotypic variation is heritable, it is appropriate to ask whether selection does operate on the phenotype; i.e., are the larval traits indeed related to fitness? Field studies on wood frogs from lowland and mountain populations suggest that this is so (Berven, 1981a). In the lowland environment the size at metamorphic climax is positively correlated with juvenile survivorship (r s = Downloaded from by guest on 15 October 2018

8 92 K. A. BERVEN AND D. E. GILL TABLE 3. Summary of the geographic variation in larval developmental traits. Traits Environmental sensitivity Length of larval period Larval body size Heritability Larval developmental time Larval body size Genetic correlations Dev. rate X body size Lowlands (Maryland) High Low , n = II, P < 0.001), however, there is no correlation between the length of the larval period and juvenile survivorship (r s = +0.04, n=ll, NS). In addition, metamorphic body size is also positively correlated with male (r = +0.85, n = 7, P < 0.01) and female (r = +0.96, n = 4, P < 0.05) size at first reproduction. Since adult body size is correlated with both male mating success (Howard, 1980; Berven, 19814) and with the number and sizes of eggs produced by females (Berven, 19826), larval metamorphic size is ultimately correlated with adult reproductive fitness. For mountain populations body size at metamorphic climax is positively correlated with juvenile survivorship (r s = +0.62, n = 6, P < 0.08) and the length of the larval period is negatively correlated with survivorship (r s = 0.64, n = 6, P < 0.07). Although sample size is small and these correlations only border on significance it is of interest to note that in contrast to lowland populations the correlations between larval traits and survivorship for juveniles in the mountains are of equivalent magnitude and of opposite sign. Finally, a natural experiment initiated in 1980 at the Beltsville, Maryland, study site provided an unusual opportunity to measure the impact of the timing of metamorphosis and metamorphic juvenile size on juvenile survival and size at first reproduction. In brief, during the summer of 1980, 20,262 juvenile frogs emerged from one lowland pond (BVI). This 1980 cohort emerged in two nonoverlapping groups separated by one week. The early metamorphic juveniles (n = 8,460) were given Mountains (Virginia) Medium Medium Tundra (Manitoba) Low High one identification mark and the later group (n = 11,802) another distinctive mark. While the timing of metamorphosis in these two cohorts differed (90 ± 1.3 vs. 102 ± 6.9 days) they did not differ in metamorphic body size (15.1 ± 0.9 mm vs ± 0.8 mm, t = 1.7, n = 205, NS). In addition to this group, 401 juveniles in a neighboring pond (BVII, 75 m away) emerged at a significantly later time (113 ± 7.0 days) than juveniles from BVI (t = 30.5, n = 12,203, P < 0.001). This BVII cohort was also significantly larger at metamorphosis than either group in BVI (17.0 ± 0.9 mm; F(2, 33 7)= 158, P < 0.001) probably because of the low density of tadpoles in that pond. Thus, three uniquely identifiable cohorts of juvenile frogs were obtained; one which metamorphosed early at a small size, a second which metamorphosed later at a comparable size and a third which metamorphosed later and significantly larger than either of the other two cohorts. Because these ponds are so close the subsequent juvenile development of all three cohorts is presumed to have occurred in the same environment. The effect of variation in larval developmental patterns on male reproductive traits was first obtained in the spring of 1981 from recovery of males breeding for the first time from each of the three cohorts. Two points are of particular interest: first, among the BVI cohorts (juveniles differing in the timing of metamorphosis but not in size) the early metamorphosing cohort had a significantly higher survivorship than the later metamorphosing cohort (0.12 (535/8,460) vs (382/11,802), Downloaded from by guest on 15 October 2018

9 GEOGRAPHIC VARIATION IN LIFEHISTORY TRAITS 93 X 2 = 103, P < 0.001), although there was no significant difference in their adult body sizes (40.9 ± 2.2 mm vs ± 2.2 mm, t = 1.3, NS). Secondly, the survivorship of the BVII cohort, which metamorphosed later and at a larger size, was significantly higher than the earlier metamorphosing BVI cohort (0.25 (50/401) vs (535/ 8,460), x 2 = 100, P < 0.001). The larger metamorphic size of the BVII cohort persisted at maturity (42.5 ±2.3 mm; F ( ) = 11.1, P < 0.001). Thus in the lowland environment of Maryland, it appears that size is more critical to survival and reproductive success than is developmental time. In summary, these preliminary results clearly demonstrate the potential importance of variation in larval patterns on future reproduction and survival. They also suggest that the relative importance of larval time and larval body size may vary between environments and imply that selection pressures may differ between environments. DISCUSSION From the research on the geographic variation in larval developmental patterns of wood frogs (summarized in Table 3) the following conclusions regarding the nature of the variability within and between populations can be drawn. First, a significant portion of the observed variation in larval period lengths and metamorphic body size and plasticity among populations is genetically based. Secondly, some of the phenotypic variation within populations is heritable and the traits are phenotypically and genetically correlated. And thirdly, larval traits are correlated with juvenile survival and adult reproductive success. Taken together the results strongly suggest that the observed patterns are locally adaptive and reflect differential selection pressures unique to each environment. It is generally thought that knowledge of the amount of additive genetic variation (h 2 ) and the nature of the genetic covariance between traits should offer insights into the nature of past selection pressures and the potential for evolutionary change. It also is commonly assumed that the heritability of traits closely associated with fitness will be low because directional selection is expected to eliminate most of the mutant genetic variation (Falconer, 1960; Lewontin, 1974). For similar reasons the genetic correlations among fitness traits are also expected to be low. For lowland and tundra populations there is close agreement between estimated levels of additive variance of larval traits and the environmental sensitivity of those traits (Table 3). For lowland larvae developmental time was very sensitive to density effects while larval body size was comparably insensitive, suggesting that larval size in Maryland is canalized, while developmental time is plastic. This was reflected in the moderate but significant heritability of developmental time compared to the low and insignificant heritability of body size (Table 3). Conversely, for tundra tadpoles larval time is canalized while body size is plastic. This is correlated with low and insignificant heritability of developmental time and a moderate and significant heritability estimate for body size (Table 3). These results suggest that selection in the lowlands has been most strong on body size and relatively weak on developmental time, while selection in tundra populations has been most strong on developmental time and relatively weak on body size. The erosion of genetic variation in a trait brought about by strong directional selection on it is also expected to diminish the genetic correlations of that trait with any other trait. Hence low genetic correlations are expected between body size and developmental time in both tundra and lowland sites because selection has been very strong on one trait at each site. The expectation is confirmed in the tundra but not in the lowlands. The mountain environment represents an interesting contrast to the patterns observed in either the lowland or tundra populations. For mountain larvae, both developmental time and larval size were relatively canalized suggesting strong selection on both size and developmental time. However, both traits showed high levels of additive genetic variance and were genetically negatively correlated (Table 3). Downloaded from by guest on 15 October 2018

10 94 K. A. BERVEN AND D. E. GILL The finding of high heritabilities in fitness traits is not new (Jinks and Broadhurst, 1963; Perrins and Jones, 1974; Ding\eetai, 1977; Istock, 1981) and a number of models (seasonally reversing selection, frequency dependent selection and others) have been offered as mechanisms for maintaining high heritabilities in fitness traits. Alternatively, Rose and Charlesworth (1981) and Rose (1982) have argued that high heritabilities may be maintained by antagonistic pleiotropy. Falconer (1960) argues that when selection is simultaneously applied to two traits their genetic correlations are eventually expected to become negative. This will occur because those pleiotropic genes that affect both characteristics in the desired direction will be fixed by natural selection and as such contribute little to the covariance of the two traits. Instead, those pleiotropic genes that affect one character positively and the other negatively will be less subject to selection and will remain at intermediate frequencies and account for most of the covariance between traits. The result is that a substantial amount of additive variation in both traits can be maintained by antagonistic pleiotropy (Rose, 1982). The high heritabilities and significant negative genetic correlations of mountain larvae are consistent with such an interpretation and support the contention that selection in the mountains is operating on both size and developmental time simultaneously. The observed shifts in the mean phenotypic expressions of larval period length and metamorphic body size among the three populations and differences in the underlying genetic structure of each doubtless result from the nature of selection in each environment, along with the environmental and developmental constraints. SmithGill and Berven (1979) have argued that metamorphosis is a developmental process which consists of both growth and differentiation. Although these two processes are highly correlated, Smith Gill and Berven argue that body size at metamorphosis will be a function of the relative balance between growth rates and differentiation rates which in turn are a function of the prevailing environment (temperature, density, food availability, etc.). High temperatures for example accelerate differentiation rates to a greater degree than they do growth rates, resulting in a shorter larval period and small body size, while under low temperature regimes differentiation rates are slowed relative to growth, resulting in a prolonged larval period and relatively larger metamorphic size. Their general prediction and one supported by the present study is that larval developmental rates and metamorphic body size should be negatively correlated. The implications to the evolution of larval patterns is that selection operating to shorten developmental time will result in an evolutionary reduction in size and viceversa. In the context of the present study the warm temperatures in the lowland environment impose rapid development and small metamorphic size. Given this environmental constraint, selection in the lowlands has been to maximize size (minimize the environmental effects) by favoring those individuals with large metamorphic size at the expense of slower developmental times and longer larval periods. In the tundra and mountain environments the cooler pond temperatures impose prolonged larval periods and large metamorphic size. In contrast to the lowland environment, selection in the tundra has favored the most rapidly developing individuals (by minimizing environmental effect) at the expense of smaller body size, while in the mountains selection has acted to maximize both developmental time and body size by minimizing the environmental effects on developmental time and maximizing the environmental effect on body size. Indeed, it could be argued that selection on growth and differentiation in the mountain population has pushed wood frogs to their physiological limits. The heritable increases in egg size in this population may represent selection to further increase metamorphic size and reduce developmental time. The differential selective advantage of either large size, fast development, or both, are borne out by available survivorship data and considerations of the biotic and abiotic Downloaded from by guest on 15 October 2018

11 GEOGRAPHIC VARIATION IN LIFEHISTORY TRAITS 95 characteristics of each environment. In the lowland environment among earlysmall, latesmall and latelarge juveniles it was the latelarge group which had the higher survivorship. Furthermore, the high correlations between larval size and survivorship versus a low and nonsignificant correlation between larval period length and survivorship supports the claim that body size is more correlated to fitness than is larval period length in the lowlands. These observations are also supported by a consideration of their environment. The presence of a large number of competitors, predators and in particular the hot summer temperatures (which increase the risk of desiccation) have doubtless been important factors favoring a large metamorphic size. On the other hand, the long and favorable growing season would place less importance on early metamorphosis. Although similar survivorship data is not available for Canadian populations, similar arguments can be made. In Canada, fast developmental rates have no doubt evolved in response to the extremely short growing season and early pond freezeup. In contrast to the lowland environment, the general lack of competitors and predators, the availability of highly productive (although pulsed) juvenile environment, and the extended solar radiation of the long days are all very conducive to rapid juvenile growth, and as a consequence, initial body size at metamorphosis would be less critical to fitness. The mountain environment clearly represents the worst of both worlds. The combination of a relatively short growing season, low productivity and generally dry conditions imposes slower juvenile growth rates and as such would favor both early metamorphosis and large size. This antagonistic selection on a developmentally constrained organism is supported by field data which demonstrate that juvenile survivorship is equally sensitive to both larval period length and larval body size. In summary, the results suggest that the observed differences in larval developmental patterns between lowland Maryland, montane Virginia and northern Canada populations of wood frogs have evolved in response to "ecological problems" imposed by their respective environments, and that the observed differences in developmental plasticity and underlying genetic structure reflect differential selection pressures. How these problems were solved is ultimately related to the physiological constraints inherent in development and the degree of compromise between the timing and size at metamorphosis allowed in each environment. In the Maryland population fitness has been maximized by evolutionary changes in size alone. In Manitoba minimum developmental rates yield maximum fitness, but in the Virginia populations, fitness has been maximized by evolutionary compromises in both size and developmental rates. This has resulted in body sizes and developmental rates in Maryland and Manitoba populations respectively which are highly canalized and genetically monomorphic. In contrast, fitness in the Virginia populations has been determined by correlated and pleiotropic effects of genes on both developmental time and body size, and both traits are equally canalized and display moderate heritabilities. These interpretations are strongly supported by characteristics of the environment and by field survivorship data. CONCLUSIONS Conclusions drawn from this study have general application to interpreting life history variation. In particular, the results of this study stress the importance of interpreting changes in life history traits relative to the constraints inherent in development (physiological, or morphological) and the constraints imposed by the environment. For example, in the present study, because of the opposing effects of growth and differentiation on larval period length and body size, and the effect of the environment on these traits, the pattern of development can be viewed as a compromise between those factors favoring large body size at metamorphosis and those factors favoring early completion of metamorphosis (see Blake, 1981; Policansky, 1982). How this compromise was achieved depended on the relative fitness of either large size or early metamorphosis in each Downloaded from by guest on 15 October 2018

12 96 K. A. BERVEN AND D. E. GILL environment. Metamorphosis is by no means unique in this regard and similar considerations would apply to any trait whose optimal expression is determined by a correlated response in another trait. Other such traits include the age and size at maturity, the number and size of offspring, photoperiod response and developmental rates, to mention a few. These results also support the general notion that fitness traits should have low levels of additive genetic variance. In general, those traits which were most closely related to fitness (based on survivorship data) did indeed have the lowest heritabilities and their expressions were relatively canalized. Although the mountain populations appeared to represent an exception, the high heritabilities appeared to be maintained by antagonistic pleiotropy. This example points out the potential pitfall of using estimates of additive genetic variance of individual traits to infer the evolutionary importance of that trait without knowing potential pleiotropic effects involved. These results also caution against the common expectation that lifehistory traits should display negative genetic correlations. Based on the present study it would appear that negative genetic correlations between fitness traits will only occur when the traits in question are constrained (either morphologically, physiologically or developmentally), are equally sensitive to fitness, and selection is operating to maximize the expression of all traits simultaneously. In contrast, negative genetic correlations will not be the rule when constraints do not exist or compromises are not necessary and fitness can be maximized by evolutionary changes in a single trait. ACKNOWLEDGMENTS This research was supported by a grant from the National Science Foundation (DEB ) and research funds from the Department of Zoology, University of Maryland. We would also like to thank the numerous individuals who assisted in the field and laboratory aspects of this research. B. Mock aided with the computer analysis. The manuscript benefited from discussions with R. Fritz, M. Hirshfield, D. Resnick and G. Wyngaard. REFERENCES Adolph, E. F The size of the body and the size of the environment in the growth of tadpoles. Biol. Bull. 61: Bellis, E. D Growth of the wood frog, Rana sylvatica. Copeia 1961:7477. Berven, K. A. 1981a. Altitudinal variation in development and reproduction in the wood frog, Rana sylvatica. Ph.D. Diss., University of Maryland. Berven, K. A Mate choice in the wood frog, Rana sylvatica. Evolution 35: Berven, K. A. 1982a. The genetic basis of altitudinal variation in the wood frog, Rana sylvatica. II. An experimental analysis of larval development. Oecologia. (1982) 52: Berven, K. A. 1982i. The genetic basis of altitudinal variation in the wood frog, Rana sylvatica. I. An experimental analysis of life history traits. Evolution. 36: Blakely, N Life history significance of sizetriggered metamorphosis in milkweed bugs (Oncopeltus). Ecology 62:5764. Collins, J. P A comparative study of the life history strategies in a community of frogs. Ph.D. Diss., University of Michigan. Dingle, H., C. K. Brown, and J. P. Hegmann The nature of genetic variance influencing photoperiodic diapause in a migrant insect, Oncopeltus fasciatus. Amer. Natur. 111: Etkin, W Metamorphosisactivating system of a frog. Science 13: Etkin, W Hormonal control of amphibian metamorphosis. In W. Etkin and L. I. Gilbert (eds.), Metamorphosis, pp Appleton CenturyCrofts, New York. Falconer, D. S Introduction to quantitative genetics. Oliver and Boyd, Edinburgh. Fishbeck, D. W A study of some phases in the ecology of Rana sylvatica (Le Conte). Ph.D. Diss., University of Minnesota. Herreid, C. F. II and S. Kinney Temperature and development of the wood frog Rana sylvatica in Alaska. Ecology 48: Hildebrand, H Notes on Rana sylvatica in the Labrador Peninsula. Copeia 3: Hinckley, M. H Notes on the development of Rana sylvatica Le Conte. Proc. Boston. Soc. Nat. Hist. 22:8595. Howard, R. D Mating behavior and mating success in wood frogs Rana sylvatica. Anim. Behav. 28: Istock, C. A The extent and consequence of heritable variation for fitness characters. In C. R. King and P. S. Dawson (eds.), Population biology: Retrospect and prospect. Columbia University Press, New York. (In press) Jinks, J. L. and P. L. Broadhurst Diallel analysis oflitter size and body weight in rats. Heredity 18: Downloaded from by guest on 15 October 2018

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