The Structure of Guppy Life Histories: The Tradeoff between Growth and Reproduction Author(s): David Reznick Source: Ecology, Vol. 64, No. 4 (Aug., 1983), pp. 862-873 Published by: Ecological Society of America Stable URL: http://www.jstor.org/stable/1937209 Accessed: 24/11/2009 00:18 Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at http://www.jstor.org/page/info/about/policies/terms.jsp. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at http://www.jstor.org/action/showPublisher?publisherCode=esa. Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printed page of such transmission. JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. Ecological Society of America is collaborating with JSTOR to digitize, preserve and extend access to Ecology. http://www.jstor.org
Transcript
The Structure of Guppy Life Histories: The Tradeoff between Growth and ReproductionAuthor(s): David ReznickSource: Ecology, Vol. 64, No. 4 (Aug., 1983), pp. 862-873Published by: Ecological Society of AmericaStable URL: http://www.jstor.org/stable/1937209Accessed: 24/11/2009 00:18
Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available athttp://www.jstor.org/page/info/about/policies/terms.jsp. JSTOR's Terms and Conditions of Use provides, in part, that unlessyou have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and youmay use content in the JSTOR archive only for your personal, non-commercial use.
Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained athttp://www.jstor.org/action/showPublisher?publisherCode=esa.
Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printedpage of such transmission.
JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range ofcontent in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new formsof scholarship. For more information about JSTOR, please contact [email protected].
Ecological Society of America is collaborating with JSTOR to digitize, preserve and extend access to Ecology.
Ecology, 64(4), 1983, pp. 862-873 Y) 1983 by the Ecological Society of America
THE STRUCTURE OF GUPPY LIFE HISTORIES: THE TRADEOFF BETWEEN GROWTH AND REPRODUCTION'
DAVID REZNICK2 Department of Biology, University of Pennsylvania,
Philadelphia, Pennsylvania 19104 USA
Abstract. This study reports on two experiments characterizing the relationship between growth and reproduction in guppies. The first experiment compares the growth of reproducing and nonre- producing siblings raised on controlled levels of food availability. Nonreproducing females have significantly more energy in somatic tissues. The bulk of this energy is in fat tissues. Standard length and "protein" do not differ significantly. The extra energy in nonreproducers is therefore devoted predominantly to energy storage, as opposed to somatic growth. A comparison of total production, however, reveals that most of the energy "saved" by not reproducing does not appear in somatic tissues. The cause of this loss is unknown.
The second experiment compares the somatic growth of different stocks of Trinidadian guppies which had previously been demonstrated to devote different quantities of energy to reproduction (Reznick 1980). Increases in the amount of energy devoted to reproduction were matched by decreases in the energy devoted to somatic tissues. Furthermore, all of the stocks have equal total production. These fish are therefore equally efficient in converting food into biomass but differ in how this biomass is allocated to growth and reproduction.
A key assumption of the theory predicting the impact of certain forms of selection on life history evolution is that an increase in the resources devoted to current reproduction reduces the future capacity to reproduce. Because fecundity is directly proportional to size in guppies, the reported tradeoff between growth and reproduction satisfies this assumption. However, such theoretical treat- ments concentrate solely on the evolution of reproductive effort. Because growth and reproduction are complementary, it is equally plausible, especially for the guppies used in these experiments, that growth rate evolved, rather than reproductive effort.
Key words: energetics; growth; life history evolution; Poecilia reticulate; reproductive costs; reproductive effort; tradeoffs.
INTRODUCTION
Theoretical treatments of life history evolution as- sume that different life history components are causal- ly related, so that an increase in a given variable will be associated with a decrease in another variable. For example, Gadgil and Bossert (1970) assume that an increase in resources devoted to reproduction results in decreased growth and survivorship.
Such tradeoffs underlie theories concerning the ef- fect on life history evolution of (1) mean age-specific differences in survivorship (Gadgil and Bossert 1970, Law 1979h, Michod 1979), (2) year-to-year variation in age-specific survivorship (e.g., Schaffer 1974), (3) density-dependent vs. density-independent population regulation (e.g., Mac Arthur and Wilson 1967), and (4) the evolution of propagule size (e.g., Wilbur 1977). In spite of the importance of elucidating these interrela- tionships among life history variables, few experimen- tal studies have attempted to do so. This study is con- cerned with one aspect of life history structure, the tradeoff between growth and reproduction.
In organisms with indeterminate growth, the rela- tionship between growth and reproduction is poten-
' Manuscript received 23 October 1981; revised 3 May 1982; accepted 17 June 1982.
2 Present address: Department of Zoology, University of Maryland, College Park, Maryland 20742 USA.
tially important because size is positively correlated with fecundity. The decreased growth associated with increased reproductive investment results in reduced future fecundity. This tradeoff thus fulfills a key as- sumption in many theoretical treatments of life history evolution, that an increase in current reproductive in- vestment reduces the future potential to reproduce (e.g., Williams 1966).
The majority of the evidence for the existence of causal relationships between life history variables are phenotypic correlations or associations. These in- clude: (1) the negative correlation between age-spe- cific fecundity and residual reproductive value ob- served among replicates within a clone of rotifers (Snell and King 1977), (2) negative correlations between so- matic growth and reproduction among individuals, within a species (Wooten 1977, Hirshfield 1980), and (3) a negative correlation between reproductive in- vestment and survivorship (Suntzeff et al. 1962, Los- chiavo 1968, Calow and Woolhead 1977, Hirshfield 1980, Browne 1982). Rose and Charlesworth's (198hz, b) discovery of negative genetic correlations between fecundity early in life and longevity and late-life fe- cundity provides more direct evidence of such trade- offs. Law's (1979a) negative correlations between fam- ily means for reproductive investment in the I st yr and reproductive investment in the 2nd yr, plant size in the 2nd yr, and probability of survival through the end of the 2nd yr imply similar genetic correlations.
August 1983 REPRODUCTIVE COSTS IN GUPPIES 863
The primary purpose of this study was to examine the relationship between growth and reproduction in the guppy (Poecilia reticulata) to determine if differ- ences in the amount of energy devoted to reproduction resulted in differences in growth. This was done from two points of view. First I examined the growth of genetically similar individuals who either had or had not reproduced. Second, I compared the growth of individuals from stocks of fish that differed genetically in the amount of energy devoted to reproduction to see if a relative decrease in reproduction was matched by an increase in somatic growth, i.e., if growth and reproduction were complementary.
The first point of view is analogous to the pheno- typic correlations referenced above in that it examines phenotypic plasticity. The second point of view ex- amines the consequences of genetic changes in growth and reproduction and hence is analogous to Rose and Charlesworth's (1981 a) quantitative genetics studies.
MATERIALS AND METHODS
Subjects (11(d experimental design
Two independent experiments were performed to determine the tradeoff between growth and reproduc- tion. In experiment I, I examined the growth of repro- ducing and nonreproducing siblings raised on con- trolled levels of food availability. The primary question was: between similar genotypes, do nonreproducing individuals have increased somatic growth relative to reproducing individuals'?
Previous treatments of this question (Alm 1959, Iles 1971) revealed no tradeoff between growth and repro- duction. These studies dealt with wild or pond-reared populations of fish and did not control food availabil- ity. The failure to observe a difference between repro- ducers and nonreproducers could be due to differences in the feeding of the two groups. For example, repro- ducing individuals may simply have eaten more to compensate for the energy devoted to reproduction. Alternatively, other factors which determined whether or not an individual reproduced, such as general health or behavioral dominance, may also have affected the relative growth of the two groups. For these reasons, my experiments dealt with isolated individuals raised on controlled food levels.
Experiment I used a randomized block design, with three levels of food availability (the "high-food" se- ries, abbreviated as Hi, H2, and H3, with Hi being the highest level) crossed with the reproducing (R) and nonreproducing (NR) treatments, for a total of six treatments per block. A block consisted of six siblings with each sib housed in its own 8-L aquarium. The six aquaria were kept on the same shelf in the laboratory. At the beginning of the experiment, an entire litter was sexed and weighed. Six females were chosen from the middle of the size distribution of the litter to minimize variation in size at the beginning of the experiment and were randomly assigned to the six treatments.
"Blocks" therefore controlled simultaneously for mi- croenvironmental differences across the laboratory, genetic differences between families of fish, and growth prior to the initiation of the experiment. The litters were between 24 and 36 d old at the initiation of the study.
The guppies used in experiment I were the F2 lab- oratory-born offspring from two localities in Trinidad, Oropuche 2 (six blocks) and Aripo 6 (six blocks), plus F2 and F3 laboratory-born domestic guppies (four blocks). The Trinidadian localities are a subset of those considered in a study of guppy life history evolution (Reznick 1980, 1982, Reznick and Endler 1982). A sec- ond series of domestic guppies (four blocks) was run at three lower levels of food availability (abbreviated as Ll, L2, and L3); the highest level of food avail- ability in this "low-food" series was lower than the lowest level of food availability in the larger study.
Experiment II compared the growth of four stocks of guppies derived from four different localities in Trinidad. Each stock differed in the proportion of con- sumed energy devoted to reproduction (Reznick 1982). The primary question was: do populations that devote different quantities of energy to reproduction exhibit complementary differences in the quantity of energy devoted to growth'? Food availability was also con- trolled in the study.
The experiment It fish were those described in Rez- nick (1982) and were derived from two types of local- ities in Trinidad, which differ in the predators that coexist with the guppies. At one type of locality, the only potential guppy predator is the killifish Riullis hartii; ii/ R ulls preys predominantly on small immature size-classes of guppies (Seghers 1973, Liley and Segh- ers 1975). At the second type of locality, guppies co- occur with the pike cichlid Crenicichla (ltal; Creniciclhla preys selectively on large, mature size-classes of gup- pies (Seghers 1973, Liley and Seghers 1975). The two Rivaulus localities (Aripo I and Quare 6) and two Cren,- icichla localities (Aripo 6 and Oropuche 2) will here- after be referred to as Riv 1, Riv 2, Cren 1, and Cren 2, respectively.
Experiment II differed from experiment I in having only two levels of food availability and only repro- ducing females, so there were only two females per block. There were 7-10 blocks per locality. All fish were 25 d old at the beginning of the experiment. All other aspects of the experiment were the same as for experiment I.
Labora tory 1 'l rering conditionss
The aquarium maintenance procedures generally followed the recommendations of Spotte (1970) and Snieszko et al. (I1974) and are detailed in Reznick (I1980).
The fish were fed twice daily, once with liver paste (Gordon 1950) and once with brine shrimp nauplii. Food availability was quantified by measuring it volumetri- cally to the nearest microlitre with a Hamilton micro-
864 DAVID REZNICK Ecology, Vol. 64, No. 4
pipette. The coefficient of variation for the dry mass of a typical ration fell between 3 and 5% (Reznick 1980: Appendix 2). Tanks were inspected for uneaten food, and a record was kept of each day that an in- dividual did not consume its full ration. Consistently poor feeders were deleted from analyses (see below).
The feeding technique was evaluated in a series of six feeding experiments, described by Reznick (1980), where food availability was varied from ad lib to bare- ly sufficient for maintaining body mass. These exper- iments demonstrated that controlling food availability in this fashion accurately regulates growth and that uncontrolled food sources (e.g., algae) make a minimal contribution to growth.
Because the energetic requirements for growth and maintenance increase with the size of the fish, food availability was periodically increased. Length and mass were measured biweekly in both experiments. The mean mass of the fish within a given food treat- ment was used to rescale food availability after each measurement. This scaling was based on the same six feeding studies, where I determined the quantity of food required to sustain a given percentage of the growth rate observed with ad lib feeding. The six feeding studies differed in the average initial masses of the fish, varying from 25 to 250 mg. The combined results of these experiments provided a series of iso- clines describing the quantity of food required (Y-axis) to sustain a given percentage of the ad lib growth rate for fish with initial wet masses ranging from 25 to 250 mg (X-axis). It was necessary to extrapolate these iso- clines to larger sizes toward the end of both experi- ments. Food availability for the experiment I fish was initially set at 50, 75, and 95% of maximum. Initial food availability in experiment II was set at 60 and 85% of maximum.
All individuals were mated once each week. In ex- periment I, NR females were mated with males that had had the tip of the anal fin removed so that they could not inseminate females but could otherwise in- teract with them in the same fashion as intact males. No NR females gave birth or became gravid during the experiment. A reproducing female and her non- reproducing sibling received the same amount of food, were measured after the birth of each litter, and were preserved immediately after the third litter. With few exceptions, the entirety of all three litters from each reproducing female was preserved for energy mea- surements. The experiment II females were only mat- ed with intact males. All other aspects of their rearing were the same as experiment I.
At the initiation of both experiments, a subset of the siblings which were not used in the experiment were preserved. These fish were used to estimate the initial energy content of the experimental fish.
Processing of preserved material
Energy content was measured for the F3 offspring and F2 females. Yolking ova plus the reproductive
tissues were dissected from the F2 females, and the gastrointestinal tract was emptied of its contents. The somatic tissues, reproductive tissues, and preserved newborn offspring were air-dried overnight at 600C. Each of these items was weighed to the nearest 0.1 mg (mass 1). The tissues were extracted with anhy- drous ether to remove triglycerides until they reached a constant mass (mass 2), ashed at 550'C in a muffle furnace, and again reweighed (mass 3). The difference between mass I and mass 2 equals the fat content of this tissue and is multiplied by 9.5 for conversion to the number of calories (Kleiber 1975). Mass 2 minus mass 3 equals the protein content and is multiplied by 5.7 to yield the number of calories (Kleiber 1975). I assumed the carbohydrate content of the lean tissues to be negligible. Similar measurements were made on liver paste and brine shrimp, giving an estimate of the energy content of a given volume of food and hence the number of calories consumed over the course of the experiment. Calories were converted to joules by multiplying by 4.184.
Energy content was also measured for the siblings of the experimental fish that were preserved when the experiment was initiated. The length-energy regres- sion line for these fish (F, 120 = 582.83, P < .0001; I2 =.83) was used to estimate the initial energy con- tent of the experimental fish.
The estimated energy content of newborn young in both experiments had to be "scaled up" to account for dry mass loss over the course of development. In wild-caught fish, the mass of developing offspring was at a maximum at the earliest stage of development and decreased by an average of 38.3% from mature ova through very late-eyed embryos. This figure repre- sents the average mass loss for the field localities con- sidered by Reznick and Endler (1982) and is inter- preted as the quantity of energy required to maintain the embryos during development. Because the percent fat did not decrease or increase significantly over the course of development, the energy content (in joules) of newborn offspring was converted into the estimated energy invested in the litter by the mother by simply multiplying the former figure by l/(I - 0.383) or 1.62.
Although in experiment I, nonreproducing females produced no offspring, all were found to contain yolked ova. These ova and the associated reproductive tis- sues were separated from the somatic tissues; separate energy measurements were made for reproductive and somatic tissues.
Statistical design and anallysis
The variables measured for comparison of the re- producing and nonreproducing females in experiment I included: (I) female length after the birth of the third litter, (2) somatic energy content, and (3) reproductive energy content. The dependent variables for the anal- ysis of energetics in experiment 1I fish included the estimated energy (in joules) devoted to reproductive and somatic tissues, and hence the total production
August 1983 REPRODUCTIVE COSTS IN GUPPIES 865
Hi
30 2
H3
26~~~~~~~~~~~~~~~~~~~~~~ 24 L
E 2 _2 2 E
0)~ ~ ~ ~~g (wes)Ae(wes
C CI,
-J~~~~~~~~~~~~~ W
20 L
18- 200 L
16- 100
14-
0 2 4 6 8 1,0 12 0 2 4 6 8 1,0 1,2
Age (weeks) Age (weeks)
Fi;. 1. Growth in length (in millimetres) and wet mass (in milligrams) for the first 12 wk of experiment I. H 1-H3 indicate the high-food series; L l-L3 indicate the low-food series. Abscissa units are number of weeks after the initiation of controlled food availability.
energy, at 6, 8, 10, and 12 wk after the initiation of the experiment. These ages were chosen because they correspond to routine measurements of female size. At 4 wk, many females had not yet matured; by 14 wk, many females had already produced three litters and had been preserved. The total production energy was estimated from the regression of wet mass on en- ergy content, using the wet masses and energy mea- surements made after the third litter as a guideline (joules = 7.36 x milligrams - 475.3; r2 = .87, P < .0001) plus the energy content of any litters born prior to the critical age, minus the estimated initial energy content. Wet mass was measured at each of the four ages. Reproductive energy was estimated as described in Reznick (1982). Somatic energy equaled the differ- ence between the above two measurements, or the energy content projected from the female's wet mass minus the energy content in the litter that she was cur- rently carrying.
The full data set for experiment I formed a three- way (2 x 3 x 16 or 2 x 3 x 4), unreplicated, mixed- model analysis of variance, with reproduction and food availability as fixed effects and blocks as a random effect. The purpose of including blocks in the design was to remove variance due to differences between block means (i.e., the effects of litters, initial size, and microenvironmental differences across the laboratory) and improve the precision for detecting differences be- tween reproducing and nonreproducing treatments. Because the experiment was unreplicated within blocks, the block x food, block x reproduction, and block x food x reproduction interactions were lumped, providing the denominator sum of squares for the remaining main effects.
Experiment II was analyzed as a two-way, fixed- effects ANOVA, with localities and food as the main effects. The initial reason for conducting experiment IL was to compare the life histories of guppies from Rivulus and Crenicichla localities. This was accom- plished with a planned comparison of the mean of Riv I and Riv 2 with the mean of Cren I and Cren 2. The remaining two locality degrees of freedom were used to test for differences between the two Crenicichla localities and between the two Riiuluis localities.
The age at which a female produced her third litter (Age 3) was a potentially important covariate in all analyses in experiment I. Because females grew throughout the experiment and litter size tended to be positively correlated with female size, Age 3 tended to be positively correlated with all energy variables. In some cases (Table 3: somatic energy and Table 5: total energy), the slopes of the Age 3-dependent vari- able regression lines were homogeneous within a level of food availability but not between food treatments; the slopes increased as food availability increased. In these cases, the covariate was nested within food availability, using three degrees of freedom. This nest- ing confounded the effects of food availability and the covariate and resulted in the food effect showing up as nonsignificant in the F table, even though a poste- riori tests indicated that all food means differed sig- nificantly. In general, the Age 3 covariate was included wherever the assumptions of the analysis of covari- ance were met.
All energy variables in experiment I were log trans- formed to conform to the assumptions of the analysis of variance.
866 DAVID REZNICK Ecology, Vol. 64, No. 4
TABLE 1. Analyses of variance of energy devoted to repro- ductive tissues. Age 3 = age (in days) at which a female produced her third litter. Means are adjusted for effects of unequal sample size, and for effects of covariates if any appear in model. R = reproducing females; NR = nonre- producing females. P = probability that the null hypothesis of equal treatment means is true.
R 749 456 238 435 NR 310 192 100 180 Food means 485 297 155
Missing va(1CS (lid outliers
Some individuals in both experiments were chroni- cally poor feeders, failing to eat their entire ration on over 20 occasions. All of these individuals were de- leted from all analyses. Some individuals either died or jumped out of their aquaria over the course of the study and were deleted from some or all analyses. Finally, four individuals in experiment II were statis- tical outliers, using the criteria of Dixon and Massey (1969), and were deleted from all analyses.
These deletions resulted in unequal sample sizes in all analyses of variance. All analyses were executed with the SAS General Linear Models Procedure (Hel- wig et al. 1979), and all F tests were based on the Type IV sums of squares, which provide exact F ratios in such circumstances. All means reported with these analyses are least squares means, which are "'esti- mates of the class or subclass means that would be expected had equal numbers been obtained" (Helwig et al. 1979:249). These means are also adjusted for the effects of covariates, if any are included in the model.
2.4
2.2-
2.0
1.8 i R~~~~~~epr
1.68
e1) 1.4 -
LuJ
1.2 a
1.0\
0.8 NonRepr
0.6
1 2 3 Food Level
FIG. 2. Energy (in kilojoules) in reproductive tissues of females in the reproducing and nonreproducing treatments of experiment 1: high-food series. Food level I is the highest. Dots indicate means; vertical lines equal + 1 SE.
RESU LTS
Experiment I
Pztects at/Woold availalbilitN'.-Food availability has
a substantial effect on growth in length and mass (Fig. 1). In this figure, H l-H3 are the three food treatments in the 16 blocks with high levels of food availability, while Ll-L3 are the three levels for the 'low-food" series. The highest level of food availability (HI) ap- proaches growth with ad lib feeding. The size achieved after 12 wk on the lowest level of food availability (L3) approximately equals the size achieved at the highest level after only 2 wk. Since at the beginning of the experiment the "low-food' individuals were larger, on the average, than the "high-food" fish, this compari- son underestimates the real differences in growth rate.
lb e ene-rgy' con tent (af reproductive tissues. -Be-
cause nonreproducing females yolk ova and hence make some energetic investment in reproduction, the first question is whether there is a significant differ- ence between reproducing and nonreproducing fe- males for this variable. For reproducing females this
August 1983 REPRODUCTIVE COSTS IN GUPPIES 867
TABLE 2. Length of female after third litter in experiment I. Abbreviations and adjustment of means are the same as in Table 1.
R 24.18 22.22 19.32 21.91 NR 23.71 21.60 19.42 21.58 Food means 23.95 21.91 19.37
variable equals the energy content of the three litters plus the reproductive tissues present in the female af- ter the third litter, while for nonreproducers it equals only the yolking ova and other reproductive tissues present at the end of the experiment. The analysis of this variable (Table 1, Fig. 2) indicates that reproduc- ing females invest approximately twice as much en- ergy in reproductive tissues as their nonreproducing counterparts; this difference is highly significant (P < .0001). Since reproducing females devote :40% of to- tal production to reproductive tissues, what then is the fate of the remaining 20% of production energy in the nonreproducing females'? In particular, does this 'ex- tra' energy result in increased somatic growth'?
Somatic growvth-.The somatic growth of reproduc- ers and nonreproducers will first be compared as the standard length after the third litter, then as the energy content of the somatic tissues. Finally, the somatic energy will be divided into the amount of energy in ether-soluble fat vs. the amount in "'protein."
The lengths of reproducing and nonreproducing fe- males are not significantly different (P > .2; Table 2), indicating that nonreproducers do not appear to de- vote any of their ""extra" energy to growing longer.
TABLE 3. Somatic energy content. Abbreviations and ad- justment of means are the same as in Table 1.
R 992 699 410 661 NR 992 678 469 678 Food means 992 686 439
In the '"high-food" series, nonreproducing females devote significantly more energy to somatic tissues than do reproducing females (Table 3, Fig. 3: bottom two portions of each bar). The bulk of the difference is due to differences in the amount of fat. Fat alone yields a significant difference between the reproducing and nonreproducing treatments, while protein does not (Table 4, Fig. 3). Since the energy content of lean tissues was always greater in nonreproducing females, a larger experiment might also reveal a significant dif- ference in protein. In summary, some of the energy that is not used in reproduction appears elsewhere, but it is devoted predominantly to fat storage as opposed to growth.
The more prominent aspect of these results is that the total production energy (reproductive plus somat- ic) is significantly greater in reproducing females (Ta- ble 5, Fig. 3). The majority of the energy that is not devoted to reproduction by nonreproducing females is thus not found in the somatic tissues and appears to be lost. Thus, while a ''tradeoff' between growth and reproduction is evident, it falls short of what is ex- pected from differences between the treatments in the energy content of the reproductive tissues.
The results for the "low-food" series generally par-
868 DAVID REZNICK Ecology, Vol. 64, No. 4
TABLE 4. Somatic energy content: fat and "protein." Abbreviations are the same as in Table 1.
allel those for the 'high-food" series (Tables 1-5), ex- cept that reproducers and nonreproducers do not dif- fer in somatic energy. This difference between series is possibly due to the much smaller sample size in the low-food treatments, or to the continuation of a trend present in the high-food" series. Within the "high- food' group, the difference in somatic energy between the reproducing treatments narrows considerably from food level I to 3 (Table 3A). The extension of this trend into the lower levels of food availability would result in little or no difference in somatic energy.
One plausible explanation for the lost" energy in nonreproducers is that the growth pattern of an indi- vidual receiving a given quantity of food is fixed and independent of reproduction. However, this result does not imply that the pattern of allocation of resources to growth and reproduction cannot be molded by natural selection. The purpose of experiment 11 is to see if there is evidence for such evolutionary changes.
Evperimnent II: interpopula tion differen ces in roI wt'll (h'id reproduction
The somatic energy, reproductive energy, and hence total energy content of each female were estimated at 6, 8, 10, and 12 wk after the initiation of the study. The original intent was to treat each of these variables with a multivariate analysis of variance, with the four consecutive measurements as the dependent vari- ables. Significant locality x time interactions preclude such an analysis for all three variables (somatic en- ergy: F., 2.64, P = .0075; reproductive: F.,M,,,= 2.00, P = .0430; total: F.8 2.54, P = .0101; Pil-
lai's trace [Helwig et al. 1979]). Interactions were tested by creating three new dependent variables equal to the difference between adjacent measurements and testing the equality of these three variables across localities (Morrison 1976:207). Because of the significant inter- actions, a separate univariate analysis was done for each dependent variable for each time period. Because four tests are conducted for each dependent variable, corresponding to the four ages when the variable is estimated, the a value for rejecting the null hypothesis of equal locality means is adjusted to 0.05/4, or 0.0125.
Crenicichla site guppies devote significantly more energy to reproduction than do Ritdlius site guppies at 6 wk and display that tendency for the remaining three ages (Table 6, Fig. 4A). However, the more prominent feature of these results is that Riv 2 falls well, below the other three localities in reproductive investment at all four ages and is significantly lower than Riv I at 8 and 10 wk (Table 6). It is the low values for Riv 2 that are primarily responsible for the overall trend between the two predator "treatments. Other noteworthy as- pects of these results are the relative increase in re- productive investment for Riv 2 fish and decrease for Cren 2 fish between weeks 10 and 12 (Fig. 4A).
The corresponding estimates for the energy in so- matic tissues are remarkably complementary to those for reproductive investment (Table 6, Fig. 4B). Riv 2 fish have greater somatic investments than the other three localities at 6, 8, and 10 wk; they are significantly greater (P < .0125) than Riv I at 8, 10, and 12 wk. Furthermore, the relative changes in Riv 2 and Cren 2 from 10 to 12 wk are matched by complementary
August 1983 REPRODUCTIVE COSTS IN GUPPIES 869
5.6j repr tis.
Ufat
4.8 - ' protein'
2.4 - Ld
1.6-
0.8-
0.0 Repr NonRepr Repr NonRepr Repr NonRepr
1 ~~~2 3 Food Level
FIG. 3. Summary of the energy content of reproductive, fat, and "protein' tissues in females in experiment I: high- food series. The height of each bar equals the mean energy content of that type of tissue.
changes in somatic energy. Riv 2 displays a relative decrease in somatic energy, while Cren 2 shows a rel- ative increase.
Total production energy does not differ significantly among the four localities across all four time periods. (Crenicichla site guppies display a nonsignificant ten- dency towards greater production energy than Rivuilis site guppies.) Therefore, all four groups are equally efficient in converting food into biomass but differ in how they allocate this biomass to growth and repro- duction.
In summary, a complementary relationship between growth and reproduction exists when different strains of fish are compared. Thus evolving a change in so- matic or reproductive investment appears to result in a corresponding change in the other variable.
DiSCUSSION
The relationship between growth and reproduction differed in the two experiments in this study. When the level of reproductive investment was artificially altered among siblings, most of the energy that would have gone into reproduction appears to have been lost; the bulk of what was not lost went into fat storage. However, when comparisons were made between stocks that devote different quantities of energy to re- production, there was a complementary relationship between the energy invested in reproductive tissues and somatic tissues, implying that evolving a change
TABLE 5. Total production energy in experiment I. Abbre- viations and adjustment of means are the same as in Table 1.
R 1757 1155 653 1096 NR 1301 891 573 874 Food means 1510 1013 607
in one of these parameters causes the opposite re- sponse in the other. The experiments thus demon- strate that the partitioning of energy between growth and reproduction can be molded by natural selection, but that within a given level of food availability this partitioning is not phenotypically plastic. The re- sources that are earmarked for reproduction, are not readily shunted into somatic growth if reproduction is prevented. It is possible that these increased fat stores could provide a tradeoff in a form not considered in this experiment, such as improved survivorship or en- hanced fecundity later in life.
The differences in the results of experiments I and II for the tradeoffs between growth and reproduction provide a caution for interpreting such studies in the context of the tradeoffs assumed by life history theory. Such theory implicitly assumes that the relationships between life history components are genetic, so that they will respond together to natural selection. Ex- periment II can be interpreted in this context; exper- iment I cannot. By this criteria, many studies reporting correlations between life history variables have been incorrectly interpreted as supporting these assump-
870 DAVID REZNICK Ecology, Vol. 64, No. 4
TABLE 6. Analyses of energy allocation in experiment II. Food availability also appears in this model. The "high" food mean is always significantly greater than the "low" food mean, while the food x locality interaction is never significant. Denominator degrees of freedom = 46 in all tests. Time units are the number of weeks after the initiation of controlled food availability.
Between predators I 5.87t 1.06NS 1.04NS 1.81NS Within Riv'uluis I 4.07NS 15.45* 11.23* 8.06* Within Crenicichla 1 1.30NS 0.79NS GOONS 5.67t
Total production energy Localities 3 O.24NS 1.46NS 0.29NS 1.99NS Planned comparisons:
Between predators 1 0.36NS 3.49NS 0.54NS 5.92t Within Rivulus I O. 15NS 1.45NS 0.27NS 0.41NS Within Crenicichil O. 0ONS 0. IONS 0.15NS 0.02NS
* P < .0125. t .0125 < P < .025. t NS = not significant.
tions. For example, Snell and King (1977) report a significant negative correlation between reproductive effort and survivorship based on variation between replicates of the same clone of rotifers raised under the same conditions. Since the replicates are geneti- cally identical, this variation is equivalent to the en- vironmental correlation in a quantitative genetics anal- ysis and hence says nothing about how this organism will respond to selection.
Similar limitations of interpretation apply to many of the remaining studies reporting life history trade- offs. In one case (Hirshfield 1980), the "tradeoff' is a negative correlation between growth and reproduction within genetically diverse organisms raised under identical circumstances. This relationship is equiva- lent to the phenotypic correlation in quantitative ge- netics. Rose and Charlesworth (198 la) and Falconer ( 1960) demonstrate that genotypic and phenotypic cor- relations can be quite different, even having opposite signs. The genotypic correlations predict the response to selection (Rose and Charlesworth 198 lb). Most of the remaining studies correlate the mean life history responses of experimental manipulations, either of re- production (Loschiavo 1968, Browne 1982) or of the environment (temperature and/or food; Calow and Woolhead 1977, Wooton 1977, Hirshfield 1980; exper- iment I in this study). Such studies are of value in characterizing phenotypic plasticity, which is a poten- tially important means of adaptation; however, they
do not necessarily predict correlated responses to se- lection, as embodied in the "tradeoffs" assumed in life history theory. Therefore, no matter how appeal- ing the results of such studies may be, they address different phenomena.
The best evidence of such tradeoffs to date are mea- surements of genetic correlations (e.g., Rose and Charlesworth 1981a) or correlated responses to selec- tion (e.g., Sokol 1970, Rose and Charlesworth 198 lb). Experiment II of this study, in examining evolutionary end-products, also contains evidence of a correlated response to selection and hence addresses the kind of "tradeoff' assumed in life history theory.
Possible explanations for the "lost energy" in experiment I
What is the fate of the extra energy in nonrepro- ductive individuals in experiment I, i.e., why is there a significant difference in total production between the reproducing and nonreproducing treatments (Fig. 3, Table 5)? One potential explanation is that the differ- ences in production are a by-product of how nonre- producing females handle unfertilized ova. For ex- ample, they could periodically extrude these ova, as reported for some strains of guppies by Spurway (1957). It was demonstrated with pilot studies that this does not occur. In these studies, virgin females were kept over nylon mesh big enough to allow ova to pass through but small enough to contain the females. These
August 1983 REPRODUCTIVE COSTS IN GUPPIES 871
individuals were observed for up to 3 mo, or longer than the adult life span of the fish in this experiment, and extruded ova were never observed.
A second potential source of lost energy might be through the continual yolking and resorption of ova. There is circumstantial evidence that guppies and oth- er poeciliids are capable of resorbing unfertilized eggs (Fraser and Renton 1940, Tavolga 1949, Thibault 1978) and have a spontaneous ovarian cycle (Siciliano 1972), although they are not capable of resorbing a litter once development begins (Meffe and Vrijenhoek 1981). The nonreproducing guppies in this experiment always ap- peared gravid and always contained a normal comple- ment of mature ova at the end of the study. If they yolked and resorbed entire clutches of eggs, at least some individuals would be expected not to contain mature ova. These fish therefore appear either to have yolked up and retained a single clutch of eggs, adding to it as they grew, or else to have continually resorbed some eggs and yolked others. In the latter case, some energy would be lost, accounting for some of the dif- ference in total production between the reproducing and nonreproducing treatments.
In normal circumstances, guppies are not likely to go uninseminated and may have not evolved the ability to recoup the energy invested in unfertilized eggs. Male guppies are promiscuous breeders (e.g., Farr and Herrnkind 1974), and females can retain sufficient sperm from a single insemination to reproduce for up to 8 mo (e.g., Winge 1922, 1937, Baerends et al. 1955). Natural populations are generally found in stable environments where, even though females often outnumber males, males are readily available and all mature females are likely to be inseminated. In 1978, 59 wild-caught females were kept in isolation in the laboratory; all of them eventually gave birth, indicating that all were carrying viable sperm. Natural selection may thus have never favored the ability to resorb ova and utilize those resources elsewhere.
Evolution (4 guppy life histories.-The presence of a growth-reproduction tradeoff in experiment II pro- vides insights concerning life history evolution in Trin- idadian guppies. Previous papers (Reznick 1980, 1982, Reznick and Endler 1982) compared the life history patterns of guppies exposed to different types of pred- ator-mediated selection. The main contrast was be- tween localities where guppies co-occur with only the killifish Rivulus hartii and localities where they co- occur with the pike cichlid Crenicichla alta and other predators. Rivulus preys predominantly on small, im- mature size-classes of guppies, while Crenicichla preys predominantly on large, mature size-classes. Creni- cichla localities are also associated with increased overall levels of predation, lower guppy population densities, and environmental factors, such as de- creased canopy cover, which possibly increase food availability to guppies relative to Rivulus localities.
A. 1.5 Reproductive energy
foRiviv c Riv 2
Cren 1
.05 ;Cren2
0.5
0.0
B. 2.0
Somatic energy
1.5
C
1.0
C.
Total energy 3.0
2.0
1.0
6 8 10 12
Age (weeks)
FIG. 4. Energy allotment by females in experiment II (means ? one standard error). Abscissa units are the number of weeks after the initiation of controlled food availability. (A) Energy content of reproductive tissues. (B) Energy con- tent of somatic tissues. (C) Total production energy.
Guppies from Crenicichla localities mature at an earlier age, reproduce more frequently, produce more and smaller offspring, and tend to devote a higher pro- portion of consumed energy to reproduction than do guppies from Rivulus localities. These life history dif- ferences correspond to the predictions of theory deal-
872 DAVID REZNICK Ecology, Vol. 64, No. 4
ing with age-specific mortality (Gadgil and Bossert 1970, Law 1979b, Michod 1979, Charlesworth 1980). One key assumption of this theory is that a tradeoff exists between current and future reproduction. This tradeoff can be achieved with the complementary re- lationship between growth and reproduction. For ex- ample, the Crenicichla pattern of increased reproduc- tive investment, especially early in life, with a corresponding reduction in somatic growth is hypoth- esized to have evolved in response to low adult sur- vivorship. Because fecundity is positively correlated with female body size (Reznick 1982), increased early reproductive investment will be associated with de- creased fecundity later in life.
These results also suggest an alternate mode of evo- lution which differs from that generally treated in the- oretical papers but has been suggested in empirical papers (e.g., Lynch 1980). Life history theory gener- ally concentrates on how certain forms of selection affect age-specific reproductive effort (e.g., Gadgil and Bossert 1970, Law 1979b, Michod 1979, Charlesworth 1980). However, the preference of Rivulus for small guppies plus the faster growth that accompanies lower reproductive investment suggest that growth rate, rather than reproductive effort, evolved. Rivulus gup- pies may have been selected for more rapid growth when vulnerable to predation, thus reducing the amount of time that they were exposed to predator-mediated mortality. The observed increase in the age at matu- ration and decrease in early reproductive investment relative to Crenicichla guppies may simply be the con- sequences associated with evolving increased early growth rates. In either case, the complementary re- lationship between somatic growth and reproduction represents a constraint that will shape the response to selection.
ACKNOWLEDGMENTS
I gratefully acknowledge the help of the members of my dissertation committee: George Constantz, Arthur Dunham, John Gillepsie, Neville Kallenbach, Robert Ricklefs, and Thomas Uzzell and thank them and my wife, Susan Snell, for their advice on all aspects of this project. I also thank Michael Hirshfield, Joseph Travis, Keith Berven, and two anonymous reviewers for their critical reviews, Jeanie Ar- ciprete for preparing and editing the manuscript, and Sandy Sage and the Academy of Natural Sciences of Philadelphia for making the facilities of the Benedict Estuarine Research Laboratory available to me while I wrote the paper. This research was partially supported by a National Science Foun- dation Predoctoral Grant and National Institutes of Health training grant GH0707 1. It was submitted in partial fulfillment of the requirements for a Ph.D. at the University of Penn- sylvania.
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