Njal Rollinson

Environmental quality predicts optimal egg size in the wild.

Parents can maximize their reproductive success by balancing the trade-off between investment per offspring and fecundity. According to theory, environmental quality influences the relationship between investment per offspring and offspring fitness, such that well-provisioned offspring fare better when environmental quality is lower. A major prediction of classic theory, then, is that optimal investment per offspring will increase as environmental quality decreases. To test this prediction, we release over 30,000 juvenile Atlantic salmon (Salmo salar) into eight wild stream environments, and we monitor subsequent growth and survival of juveniles. We estimate the shape of the relationship between investment per offspring (egg size) and offspring fitness in each stream. We find that optimal egg size is greater when the quality of the stream environment is lower (as estimated by a composite index of habitat quality). Across streams, the mean size of stream gravel and the mean amount of incident sunlight are the most important individual predictors of optimal egg size. Within streams, juveniles recaptured in stream subsections that featured larger gravels and greater levels of sunlight also grew relatively quickly, an association that complements our cross-stream analyses. This study provides the first empirical verification that environmental quality alters the relationship between investment per offspring and offspring fitness, such that optimal investment per offspring increases as environmental quality decreases.

Are all eggs created equal? Food availability and the fitness trade-off between reproduction and immunity

Summary 1. Reproduction and immune function are critical processes, but organisms can rarely optimize both traits. Resultant reproduction–immunity trade-offs may be ‘facultative’, occurring only when resources are scarce, or they may be ‘obligate’, occurring regardless of resource availability. 2. Previous research has tested for the ‘facultative’ or ‘obligate’ nature of reproduction–immunity trade-offs by measuring resource allocation (e.g. follicle size). However, measuring resource allocation alone may be insufficient when gauging the fitness consequences of reproduction–immunity trade-offs because the number and quality of eggs or offspring trade off with one another. 3. We used the Texas field cricket (Gryllus texensis) to provide the most direct test to date of whether a fitness trade-off between these two traits is ‘facultative’ or ‘obligate’. We used a factorial design to manipulate food availability and immune status throughout adulthood. We then estimated lifetime fecundity, hatching success and their product (reproductive success), and we also measured several aspects of offspring quality (e.g. egg size and protein content, and hatchling size and energy stores). 4. A reproduction–immunity trade-off was ‘obligate’ in this species because immune challenge reduced reproductive success estimates regardless of food availability. Females with unlimited food were more fecund and produced more and larger hatchlings, but neither food availability nor immune status affected egg size, egg phenoloxidase activity, incubation duration, hatching success or hatchling energy stores. We observed a trade-off between offspring size and number – females favouring offspring size over fecundity produced fewer hatchlings, but their hatchlings were of higher quality (larger and more robust). 5. By demonstrating that not all eggs are created equal, we provide key insight into the role of reproductive allocation in the fitness trade-off between reproduction and immunity.

The relationship between offspring size and fitness: integrating theory and empiricism

How parents divide the energy available for reproduction between size and number of offspring has a profound effect on parental reproductive success. Theory indicates that the relationship between offspring size and offspring fitness is of fundamental importance to the evolution of parental reproductive strategies: this relationship predicts the optimal division of resources between size and number of offspring, it describes the fitness consequences for parents that deviate from optimality, and its shape can predict the most viable type of investment strategy in a given environment (e.g., conservative vs. diversified bet-hedging). Many previous attempts to estimate this relationship and the corresponding value of optimal offspring size have been frustrated by a lack of integration between theory and empiricism. In the present study, we draw from C. Smith and S. Fretwells classic model to explain how a sound estimate of the offspring size--fitness relationship can be derived with empirical data. We evaluate what measures of fitness can be used to model the offspring size--fitness curve and optimal size, as well as which statistical models should and should not be used to estimate offspring size--fitness relationships. To construct the fitness curve, we recommend that offspring fitness be measured as survival up to the age at which the instantaneous rate of offspring mortality becomes random with respect to initial investment. Parental fitness is then expressed in ecologically meaningful, theoretically defensible, and broadly comparable units: the number of offspring surviving to independence. Although logistic and asymptotic regression have been widely used to estimate offspring size-fitness relationships, the former provides relatively unreliable estimates of optimal size when offspring survival and sample sizes are low, and the latter is unreliable under all conditions. We recommend that the Weibull-1 model be used to estimate this curve because it provides modest improvements in prediction accuracy under experimentally relevant conditions.

Thermoregulation When the Growing Season Is Short: Sex-Biased Basking Patterns in a Northern Population of Painted Turtles (Chrysemys picta)

Abstract In reptiles, thermoregulation is important because it alters the rate of many physiological processes. Thermoregulation may be especially important to reproductive females that inhabit regions where the growing season is short, because the amount of thermal energy experienced during the season may limit the amount of energy devoted to egg production. We studied basking behavior of Painted Turtles (Chrysemys picta) in Algonquin Park, Ontario, during the period of follicular recrudescence, a time of year when females allocate energy to developing follicles. Based on the notion that females bask (in part) to increase the amount of energy they allocate to developing follicles, we tested whether basking duration was greater in females than in males. Between 14 and 21 August 2003, we found that females basked longer than males on three of seven days, but males never basked significantly longer than females. Within sex, male but not female body size was positively related to basking duration. Our study suggests that the energetic demands of egg production result in an increased basking duration for females in this northern population. Males may bask to reach a certain temperature then return to water because of potential mating opportunities. Future studies should combine body temperature measurements with behavioral observations to elucidate further the reasons for sex-biased basking.

The positive correlation between maternal size and offspring size: fitting pieces of a life‐history puzzle

The evolution of investment per offspring (I) is often viewed through the lens of the classic theory, in which variation among individuals in a population is not expected. A substantial departure from this prediction arises in the form of correlations between maternal body size and I, which are observed within populations in virtually all taxonomic groups. Based on the generality of this observation, we suggest it is caused by a common underlying mechanism. We pursue a unifying explanation for this pattern by reviewing all theoretical models that attempt to explain it. We assess the generality of the mechanism upon which each model is based, and the extent to which data support its predictions. Two classes of adaptive models are identified: models that assume that the correlation arises from maternal influences on the relationship between I and offspring fitness [w(I)], and those that assume that maternal size influences the relationship between I and maternal fitness [W(I)]. The weight of evidence suggests that maternal influences on w(I) are probably not very general, and even for taxa where maternal influences on w(I) are likely, experiments fail to support model predictions. Models that assume that W(I) varies with maternal size appear to offer more generality, but the current challenge is to identify a specific and general mechanism upon which W(I) varies predictably with maternal size. Recent theory suggests the exciting possibility that a yet unknown mechanism modifies the offspring size–number trade‐off function in a manner that is predictable with respect to maternal size, such that W(I) varies with size. We identify two promising avenues of inquiry. First, the trade‐off might be modified by energetic costs that are associated with the initiation of reproduction (‘overhead costs’) and that scale with I, and future work could investigate what specific overhead costs are generally associated with reproduction and whether these costs scale with I. Second, the trade‐off might be modified by virtue of condition‐dependent offspring provisioning coupled with metabolic factors, and future work could investigate the proximate cause of, and generality of, condition‐dependent offspring provisioning. Finally, drawing on the existing literature, we suggest that maternal size per se is not causatively related to variation in I, and the mechanism involved in the correlation is instead linked to maternal nutritional status or maternal condition, which is usually correlated with maternal size. Using manipulative experiments to elucidate why females with high nutritional status typically produce large offspring might help explain what specific mechanism underlies the maternal‐size correlation.

Persistent directional selection on body size and a resolution to the paradox of stasis

Directional selection on size is common but often fails to result in microevolution in the wild. Similarly, macroevolutionary rates in size are low relative to the observed strength of selection in nature. We show that many estimates of selection on size have been measured on juveniles, not adults. Further, parents influence juvenile size by adjusting investment per offspring. In light of these observations, we help resolve this paradox by suggesting that the observed upward selection on size is balanced by selection against investment per offspring, resulting in little or no net selection gradient on size. We find that trade‐offs between fecundity and juvenile size are common, consistent with the notion of selection against investment per offspring. We also find that median directional selection on size is positive for juveniles but no net directional selection exists for adult size. This is expected because parent–offspring conflict exists over size, and juvenile size is more strongly affected by investment per offspring than adult size. These findings provide qualitative support for the hypothesis that upward selection on size is balanced by selection against investment per offspring, where parent–offspring conflict over size is embodied in the opposing signs of the two selection gradients.

Marking Nests Increases the Frequency of Nest Depredation in a Northern Population of Painted Turtles (Chrysemys picta)

Abstract Predators use visual and olfactory cues to locate turtle nests. Since 1999, we marked Painted Turtle (Chrysemys picta) nests at a long-term study site by inserting Popsicle™ sticks part way into the nest cavity. Because nest-marking provides a cue to potential predators, we tested whether nest-marking increases nest depredation rates. During the nesting season, 15 artificial nest pairs (N  =  30 artificial nests in total) were created by digging and refilling holes (presumably emulating nest excavation by turtles) at a nesting site. Nests in each pair were 45 cm apart, but only one nest in each pair was marked with a Popsicle™ stick, and no eggs were placed in either hole. After one week, depredation was observed in nine of the 15 nest pairs, and all depredation events were directed towards marked nests. A Binomial Test revealed that this pattern was significantly nonrandom. It is possible that predators were responding to olfactory cues left by Popsicle™ sticks, and given that mammalian predators are common at our study site, we cannot rule out the possibility that such olfactory-oriented predators depredated artificial nests. However, we suspect that Common Ravens (Corvus corax) and American Crows (Corvus brachyrhynchos; nest predators that are visually oriented) were the primary predators in this study. Future experiments should use turtle eggs in both marked and unmarked nests to evaluate whether the markers represent a significant mortality factor for Painted Turtle eggs.

Risk Assessment of Inbreeding and Outbreeding Depression in a Captive‐Breeding Program

Captive-breeding programs can be implemented to preserve the genetic diversity of endangered populations such that the controlled release of captive-bred individuals into the wild may promote recovery. A common difficulty, however, is that programs are founded with limited wild broodstock, and inbreeding can become increasingly difficult to avoid with successive generations in captivity. Program managers must choose between maintaining the genetic purity of populations, at the risk of inbreeding depression, or interbreeding populations, at the risk of outbreeding depression. We evaluate these relative risks in a captive-breeding program for 3 endangered populations of Atlantic salmon (Salmo salar). In each of 2 years, we released juvenile F(1) and F(2) interpopulation hybrids, backcrosses, as well as inbred and noninbred within-population crosstypes into 9 wild streams. Juvenile size and survival was quantified in each year. Few crosstype effects were observed, but interestingly, the relative fitness consequences of inbreeding and outbreeding varied from year to year. Temporal variation in environmental quality might have driven some of these annual differences, by exacerbating the importance of maternal effects on juvenile fitness in a year of low environmental quality and by affecting the severity of inbreeding depression differently in different years. Nonetheless, inbreeding was more consistently associated with a negative effect on fitness, whereas the consequences of outbreeding were less predictable. Considering the challenges associated with a sound risk assessment in the wild and given that the effect of inbreeding on fitness is relatively predictable, we suggest that risk can be weighted more strongly in terms of the probable outcome of outbreeding. Factors such as genetic similarities between populations and the number of generations in isolation can sometimes be used to assess outbreeding risk, in lieu of experimentation.

Widespread reproductive variation in North American turtles: temperature, egg size and optimality

Theory predicts the existence of an optimal offspring size that balances the trade-off between offspring fitness and offspring number. However, in wild populations of many species, egg size can still vary from year to year for unknown reasons. Here, we hypothesize that among-year variation in population mean egg size of freshwater turtles is partly a consequence of their gonadal sensitivity to seasonal temperatures, a physiological mechanism which principally functions to synchronize reproduction with a favorable time of year. As part of this process, among-year variation in seasonal temperatures modifies the extent of egg follicle development, and this may translate into variation in mean egg size among years (both at the individual and population level). To test this hypothesis, we applied an information-theoretic approach to model relationships between mean egg mass and the temperatures experienced during discrete periods of follicular development in wild populations of three turtle species (Chrysemys picta, Chelydra serpentina, Glyptemys insculpta) over 12 consecutive years. Because follicular development occurs in the fall for C. serpentina and G. insculpta, whereas it occurs both in the fall and spring for C. picta, we expected only fall temperatures would explain egg size variation in C. serpentina and G. insculpta, whereas both fall and spring temperatures would correlate with egg size variation in C. picta. These predictions were upheld. We then compared among-year variation in within-female egg and clutch sizes of each species in order to evaluate whether such variation might still be consistent with some tenets of optimal egg size theory. In all three species, we found that clutch sizes vary more than egg sizes in spite of temperature-induced egg size variation, and this pattern of relatively high clutch-size variation matches theoretical predictions. Future work should explore the roles of direct and indirect (i.e., nutritional) influences of temperature on egg size in natural settings.

Sources and Significance of Among-Individual Reproductive Variation in a Northern Population of Painted Turtles (Chrysemys picta)

Abstract Painted Turtles (Chrysemys picta) are often used to test life-history theory. However, within populations, the factors that contribute to among-individual variation in egg size and clutch size are poorly understood, and an understanding of the biotic and abiotic parameters that contribute to this variation is important when framing patterns of maternal investment in a life-history context. We examined proximate sources of reproductive variation in a northern population of Painted Turtles, we attempted to frame these sources of variation in a life-history context, and we evaluate which optimality model most adequately explains patterns of reproductive allocation in populations of small-bodied turtles. We used multiple linear regression on data from 168 first clutches of marked females that nested at a long-term study site in Algonquin Park, Ontario, Canada, in 2004. We found that mean egg mass was positively related to maximum plastron length (MPL) and female age, and negatively related to clutch size and water temperature prior to oviposition. Clutch size was positively related to MPL and carapace height, and negatively related to mean egg mass, and the number of clutches laid in the season. Body size (MPL) was the most important predictor of each reproductive parameter, and residual analysis indicated that egg mass was more conserved than clutch size across the range of female body sizes sampled in this study. Thus, egg size may be optimized as a body size-specific function, and in light of this, we suggest that ‘phenotype-habitat matching’ may occur in C. picta. If a females phenotype (e.g., body size) influences the selective environment of her eggs and hatchlings (e.g., if larger females generally nest farther away from water), then the optimal strategy of maternal investment should vary among maternal phenotypes. The positive correlation between egg mass and body size that was observed in the present study can be explained in adaptive terms under hypotheses based on the concept of phenotype–habitat matching.