The ontogeny of postmaturation resource allocation in turtles

Resource-allocation decisions vary with life-history strategy, and growing evidence suggests that long-lived endothermic vertebrates direct resources toward growth and self-maintenance when young, increasing allocation toward reproductive effort over time. Few studies have tracked the ontogeny of resource allocation (energy, steroid hormones, etc.) in long-lived ectothermic vertebrates, limiting our understanding of the generality of life-history strategies among vertebrates. We investigated how reproductively mature female painted turtles (Chrysemys picta) from two distinct age classes allocated resources over a 4-yr period and whether resource-allocation patterns varied with nesting experience. We examined age-related variation in body size, egg mass, reproductive frequency, and yolk steroids and report that younger females were smaller and allocated fewer resources to reproduction than did older females. Testosterone levels were higher in eggs from younger females, whereas eggs from second (seasonal) clutches contained higher concentrations of progesterone and estradiol. These allocation patterns resulted in older, larger females laying larger eggs and producing second clutches more frequently than their younger counterparts. We conclude that resource-allocation patterns do vary with age in a long-lived ectotherm.     

Adaptive egg size plasticity for larval competition and its limits in the seed beetle Callosobruchus chinensis

Life‐history theory predicts that females who experienced stressful conditions, such as larval competition or malnutrition, should increase their investment in individual offspring to increase offspring fitness (the adaptive parental hypothesis). In contrast, it has been shown that when females were reared under stressful conditions, they become smaller, which consequently decreases egg size (the parental stress hypothesis). To test whether females adjust their egg volume depending on larval competition, independent of maternal body mass constraint, we used a pest species of stored adzuki beans, Callosobruchus chinensis (L.) (Coleoptera: Chrysomelidae: Bruchinae). The eggs of females reared with competitors were smaller than those of females reared alone, supporting the parental stress hypothesis; however, correcting for female body size, females reared with competitors produced larger eggs than those reared in the absence of competition, supporting the adaptive parental hypothesis, as predicted. The phenotypic plasticity in females' investment in each offspring in stressful environments counteracts the constraint of body size on egg size.     

Maternal condition, yolk androgens and offspring performance: a supplemental feeding experiment in the lesser black-backed gull (Larus fuscus)

It has been proposed that the maternal androgens in avian egg yolk enhance offspring fitness by accelerating growth and improving competitive ability. Because egg quality is strongly influenced by maternal condition, we predicted that females in good condition would produce high-quality eggs with relatively high androgen content. We experimentally enhanced maternal condition by supplementary feeding lesser black-backed gulls (Larus fuscus) during egg formation and compared the concentrations of androstenedione (A4), 5alpha-dihydrotestosterone (DHT) and testosterone (T) in their eggs with those in eggs laid by control females. We also measured circulating levels of T in females immediately after laying. Egg androgens could affect offspring performance directly through chick development and/or indirectly through changes in the competitive ability of a chick relative to its siblings. To avoid confounding these two routes, and to separate effects operating through the egg itself with those operating through experimental changes in parental chick rearing capacity, we fostered eggs from both maternal treatment groups singly into the nests of unmanipulated parents. Contrary to expectation, mothers with experimentally enhanced body condition laid eggs with lower levels of androgens, while exhibiting higher circulating T concentrations post-laying. Despite these lower levels of egg androgen, offspring hatched from eggs laid by mothers in good condition did not show reduced growth or survival when reared in the absence of sibling competition. Our results demonstrate that yolk androgen concentrations vary with the body condition of the female at the time of egg formation and that females in good condition reduced the yolk androgen content of their eggs without altering offspring performance.     

Embryonic death is linked to maternal identity in the leatherback turtle (Dermochelys coriacea)

Leatherback turtles have an average global hatching success rate of ~50%, lower than other marine turtle species. Embryonic death has been linked to environmental factors such as precipitation and temperature, although, there is still a lot of variability that remains to be explained. We examined how nesting season, the time of nesting each season, the relative position of each clutch laid by each female each season, maternal identity and associated factors such as reproductive experience of the female (new nester versus remigrant) and period of egg retention between clutches (interclutch interval) affected hatching success and stage of embryonic death in failed eggs of leatherback turtles nesting at Playa Grande, Costa Rica. Data were collected during five nesting seasons from 2004/05 to 2008/09. Mean hatching success was 50.4%. Nesting season significantly influenced hatching success in addition to early and late stage embryonic death. Neither clutch position nor nesting time during the season had a significant affect on hatching success or the stage of embryonic death. Some leatherback females consistently produced nests with higher hatching success rates than others. Remigrant females arrived earlier to nest, produced more clutches and had higher rates of hatching success than new nesters. Reproductive experience did not affect stage of death or the duration of the interclutch interval. The length of interclutch interval had a significant affect on the proportion of eggs that failed in each clutch and the developmental stage they died at. Intrinsic factors such as maternal identity are playing a role in affecting embryonic death in the leatherback turtle.     

Ovarian dynamics, egg size, and egg number in relation to temperature and mating status in a butterfly

Although the temperature‐size rule, that is, an increase in egg (and body) size at lower temperatures, applies almost universally to ectotherms, the developmental mechanisms underlying this consistent pattern of phenotypic plasticity are hitherto unknown. By investigating ovarian dynamics and reproductive output in the tropical butterfly Bicyclus anynana (Butler) (Lepidoptera: Nymphalidae: Satyrinae) in relation to oviposition temperature and mating status, we tested the relevance of several competing hypotheses for temperature‐mediated variation in egg size and number. As expected, females ovipositing at a lower temperature laid fewer but larger eggs than those ovipositing at a higher temperature. Despite pronounced differences in egg‐laying rates, oocyte numbers were equal across temperatures at any given time, while oocyte size increased at the lower temperature. In contrast, there were greatly reduced oocyte numbers in mated compared to virgin females. Our results indicated that temperature‐mediated plasticity in egg size cannot be explained by reduced costs of somatic maintenance at lower temperatures, enabling the allocation of more resources to reproduction (reproductive investment was higher at the higher temperature). Furthermore, there was no indication for delayed oviposition (no accumulation of oocytes at the lower temperature, in contrast to virgin females). Rather, low temperatures greatly reduced the oocyte production (i.e., differentiation) rate and prolonged egg‐maturation time, causing low egg‐laying rates. Our data thus suggested that oocyte growth is less sensitive to temperature than oocyte production, resulting in a lower number of larger eggs at lower temperatures.     

Embryonic temperature affects metabolic compensation and thyroid hormones in hatchling snapping turtles.

Temperature acclimation of adult vertebrates typically induces changes in metabolic physiology. During early development, such metabolic compensation might have profound consequences, yet acclimation of metabolism is little studied in early life stages. We measured the effect of egg incubation temperature on resting metabolic rate (RMR) and blood thyroid hormone levels of hatchling snapping turtles (Chelydra serpentina). Like many reptiles, snapping turtles have temperature-dependent sex determination (TSD), in which embryonic temperature determines sex. Therefore, we designed the experiments to separately measure effects of temperature and of sex on the response variables. We incubated eggs in the laboratory at 21. 5 degrees, 24.5 degrees, 27.5 degrees, and 30.5 degrees C, producing both sexes, all males, both sexes, and all females, respectively. Hatchling RMR, when measured at a common temperature (either 25 degrees or 31 degrees C), was negatively correlated with egg temperature in both males and females, such that RMR of turtles from 21.5 degrees C-incubated eggs averaged 160% that of turtles from 30.5 degrees C-incubated eggs. These results indicate that egg temperatures induced positive metabolic compensation in both sexes. Thyroid hormone levels of hatchlings showed similar correlations with egg temperature; thyroxine level of turtles from 21.5 degrees C-incubated eggs averaged 220% that of turtles from 30.5 degrees C-incubated eggs. To examine the possibility that thyroid hormones contribute to positive metabolic compensation, we added triiodothyronine to eggs during mid-incubation. RMR of hatchlings from these treated eggs averaged 131% that of controls, consistent with the previous possibility. Moreover, the effects of embryonic temperature on metabolic physiology, in combination with effects on sex, can result in differences in RMR and thyroid hormone levels between male and female hatchling turtles. Such differences may be important to the ecology and evolution of TSD.     

Body size-specific maternal effects on the offspring environment shape juvenile phenotypes in Atlantic salmon

Positive associations between maternal investment per offspring and maternal body size have been explained as adaptive responses by females to predictable, body size-specific maternal influences on the offspring’s environment. As a larger per-offspring investment increases maternal fitness when the quality of the offspring environment is low, optimal egg size may increase with maternal body size if larger mothers create relatively poor environments for their eggs or offspring. Here, we manipulate egg size and rearing environments (gravel size, nest depth) of Atlantic salmon (Salmo salar) in a 2 × 2 × 2 factorial experiment. We find that the incubation environment typical of large and small mothers can exert predictable effects on offspring phenotypes, but the nature of these effects provides little support to the prediction that smaller eggs are better suited to nest environments created by smaller females (and vice versa). Our data indicate that the magnitude and direction of phenotypic differences between small and large offspring vary among maternal nest environments, underscoring the point that removal of offspring from the environmental context in which they are provisioned in the wild can bias experimentally derived associations between offspring size and metrics of offspring fitness. The present study also contributes to a growing literature which suggests that the fitness consequences of egg size variation are often more pronounced during the early juvenile stage, as opposed to the egg or larval stage.     

The importance of energetic versus pelvic constraints on reproductive allocation by the eastern fence lizard (Sceloporus undulatus)

In ectothermic species, females often produce larger eggs in colder environments. Models based on energetic constraints suggest that this pattern is an adaptation to compensate for the slower growth of offspring in the cold. Yet, females in cold environments also tend to be larger than females in warm environments. Consequently, thermal clines in egg size could be caused by pelvic constraints, which stem from the inability of large eggs to pass through a small pelvic aperture. Models based on energetic constraints and models based on pelvic constraints predict similar relationships between maternal size and egg size. However, pelvic constraints should produce these relationships both within and among populations, whereas energetic constraints would not necessarily do so. If pelvic constraints are important, we might also expect small females to compensate by producing eggs that are relatively rich in lipids (i.e. high energy density). The present study aimed to assess whether energetic or pelvic constraints generate geographical variation in egg size of the lizard Sceloporus undulatus . Pelvic width is very highly correlated with body length in S. undulatus , making maternal size a suitable measure of pelvic constraint. Although maternal size and egg mass (dry and wet) covaried among populations, these variables were generally not related within populations. Energetic density of eggs tended to increase with decreasing egg mass (dry and wet), but this relationship was strongest in populations where no relationship between maternal size and egg mass was observed. Our results do not support the pelvic constraint model and thus indicate energetic constraints play a greater role in generating geographical variation in egg size.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 91 , 513–521.     

Variation in body size in the giant rhinoceros beetle Trypoxylus dichotomus is mediated by maternal effects on egg size

1. The egg size of insects can vary depending on maternal body size or resource status, and it may influence offspring body size by determining initial resource level. 2. The giant rhinoceros beetle Trypoxylus dichotomus exhibits considerable variation in body size, some of which is attributed to the variation in larval food (humus) quality, although a substantial amount of variation in body size remains unexplained. In the present study, changes in the egg size and offspring body size in response to several maternal variables were examined (i.e. body size, age, and, nutritional status). 3. Nutritional intake of the females during the adult stage did not affect the egg size. Larvae hatched from small eggs partially recovered from the initial disadvantage during their ontogenetic processes by increasing growth rate (i.e. compensatory growth); however, there was still a positive relationship between egg size and pupal body size. 4. Older females produced small eggs, but because of compensatory growth, the pupae were no longer small. By contrast, due to a lack of compensatory growth, small females produced small eggs as well as small pupae. 5. These results suggest that maternal body size affects offspring body size through effects on egg size. This transgenerational effect may account for some of the variation in adult body size of T. dichotomus.     

Multiple paternity in egg clutches of hawksbill turtles (Eretmochelys imbricata)

We present the first data collected on the genetic mating system of the hawksbill turtle Eretmochelys imbricata, the only marine turtle not studied to date. We examined paternity within 12 egg clutches from ten female hawksbill turtles from Sabah Turtle Islands, Malaysia. A total of 375 hatchlings were analysed using five microsatellite markers. Results demonstrated that clutches from two out of ten females were sired by multiple males (maximum of two). Although at a low frequency, observation of multiple paternity indicates that hawksbill turtles exhibit the same genetic mating system (polyandry) as observed for other species of marine turtles. Consistent paternity across multiple clutches laid by individual females in one breeding season supports the hypothesis that sperm are stored from mating prior to nesting and are then used to fertilize all subsequent clutches of eggs that season.     

Individual Variation in Trophic Egg Production: Evidence for Maternal Manipulation in Response to Resource and Competition Levels

Females of the subsocial shield bug Parastrachia japonensis (Heteroptera: Parastrachiidae) incorporate trophic eggs (nutritive eggs) into their egg mass. Considerable variation occurs among females in trophic egg number and the proportion of an egg mass that is composed of trophic eggs. Because trophic eggs are essential to the development and survival of young, this variation could significantly impact female fitness. We tested the hypothesis that trophic egg abundance is induced by maternal phenotype (weight, body size) and resource exposure. We predicted that resource limitations would cause females to produce fewer fertile eggs and more trophic eggs and that larger and heavier females would produce more of each egg type. Females ovipositing early in the season are exposed to different resource conditions than those that oviposit late. Thus, we compared egg production patterns between these two groups and several other factors related to nesting. No correlation was seen between body size and trophic egg abundance, or, indeed, egg production, overall; however, heavier females produced heavier egg masses. Counter to our prediction, late females, which had greater access to food, produced significantly more total eggs, fewer fertile eggs, and more trophic eggs than early females. A binomial generalized linear model analysis indicated that the factors most correlated with the percentage of an egg mass destined to become trophic eggs were resource abundance, resulting from early or late oviposition, and distance of the nest from the host tree, with closer females producing more trophic eggs. The findings support our hypothesis that resource availability and, to a lesser extent, maternal phenotype affect trophic egg abundance.     

Egg size plasticity corresponding to maternal food conditions in an annual fish,Ayu <Emphasis Type="Italic">Plecoglossus altivelis</Emphasis>

The classic model of Smith and Fretwell predicts that the optimal egg size will vary according to the shape of the relationship between offspring size and offspring fitness, which may vary among environments. Adaptive significance of intrapopulation egg size variation was examined using Ayu (Plecoglossus altivelis). The species has an annual and migratory life history. Fish under controlled rearing conditions become sexually mature with a trend that smaller females produced larger eggs later in the season. Observed egg size variation was explained by the maternal specific growth rate, which was composed of maternal body size and growing period. Hatchlings from larger eggs had a larger notochord length, larger yolk-sac and grew faster. Such offspring traits provide general advantages of increased larval size, which confer competitive ability for assuring early survivorship. In conclusion, egg size plasticity in Ayu suggests higher offspring fitness through enhancement of their accessibility to food.     

Temperature‐mediated trade‐offs and changes in life‐history integration in two slipper limpets (Gastropoda: Calyptraeidae) with planktotrophic development

Intraspecific variation in egg size and hatching size, and the genetic and environmental trade‐offs that contribute to variation, are the basis of the evolution of life histories. The present study examined both univariate and multivariate temperature‐mediated plasticity of life‐history traits, as well as temperature‐mediated trade‐offs in egg size and clutch size, in two planktotrophic species of marine slipper limpets, Crepidula. Previous work with two species of Crepidula with large eggs and lecithotrophic development has shown a significant effect of temperature on egg size and hatching size. To further examine the effect of temperature on egg size in Crepidula, the effects of temperature on egg size and hatching size, as well as the possible trade‐offs with other the life‐history features, were examined for two planktotrophic species: Crepidula incurva and Crepidula cf. marginalis. Field‐collected juveniles were raised at 23 or 28 °C and egg size, hatching size, capsules/brood, eggs/capsule, time to hatch, interbrood interval, and final body weight were recorded. Consistent with results for the lecithotrophic Crepidula, egg size and hatching size decreased with temperature in the planktotrophic species. The affects of maternal identity and individual brood account for more than half of the intraspecific variation in egg size and hatching size. Temperature also showed a significant effect on reproductive rate, with time to hatch and interbrood interval both decreasing with increasing temperature. However, temperature had contrasting effects on the number of offspring. Crepidula cf. marginalis has significantly more eggs/capsule and therefore more eggs per brood at 28 °C compared to 23 °C, although capsules/brood did not vary with temperature. Crepidula incurva, on the other hand, produced significantly more capsules/brood and more eggs per brood at the lower temperature, whereas the number of eggs/capsule did not vary with temperature. The phenotypic variance–covariance matrix of life‐history variables showed a greater response to temperature in C. incurva than in C. cf. marginalis, and temperature induced trade‐offs between offspring size and number differ between the species. These differences suggest that temperature changes as a result of seasonal upwelling along the coast of Panama will effect the reproduction and evolution of life histories of these two co‐occurring species differently. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.     

Microhabitat selection by sea turtles in a dynamic thermal marine environment

1. Reproductive fitness is often compromised at the margins of a species' range due to sub-optimal conditions. 2. Set against this backdrop, the Mediterranean's largest loggerhead sea turtle (Caretta caretta) rookery at Zakynthos (Greece) presents a conundrum, being at a very high latitude for this species, yet hosting a high concentration of nesting. 3. We used visual surveys combined with global positioning system (GPS) tracking to show that at the start of the breeding season, individuals showed microhabitat selection, with females residing in transient patches of warm water. As the sea warmed in the summer, this selection was no longer evident. 4. As loggerhead turtles are ectothermic, this early season warm-water selection presumably speeds up egg maturation rates before oviposition, thereby allowing more clutches to be incubated when sand conditions are optimal during the summer. 5. Active selection of warm waters may allow turtles to initiate nesting at an earlier date.     

Temperature dependence of evolutionary diversification: differences between two contrasting model taxa support the metabolic theory of ecology

Biodiversity patterns are largely determined by variation of diversification rates across clades and geographic regions. Although there are multiple reasons for this variation, it has been hypothesized that metabolic rate is the crucial driver of diversification of evolutionary lineages. According to the metabolic theory of ecology (MTE), metabolic rate – and consequently speciation – is driven mainly by body size and environmental temperature. As environmental temperature affects metabolic rate in ecto‐ and endotherms differently, its impact on diversification rate should also differ between the two types of organisms. Employing two independent approaches, we analysed correlates of speciation rates and, ultimately, net diversification rates for two contrasting taxa: plethodontid salamanders and carnivoran mammals. Whereas in the ectothermic plethodontids speciation rates positively correlated with environmental temperature, in the endothermic carnivorans a reverse, negative correlation was detected. These findings comply with predictions of the MTE and suggest that similar geographic patterns of biodiversity across taxa (e.g. ecto‐ and endotherms) might have been generated by different ecological and evolutionary processes.     

Optimal offspring provisioning when egg size is "constrained": a case study with the painted turtle Chrysemys picta

Classic egg size theory predicts that, in a given environment, there is a level of maternal investment per offspring that will maximize maternal fitness. However, positive correlations among egg size and female body size are observed within populations in diverse animal taxa. A popular explanation for this phenomenon is that, in some populations, morphological constraints on egg size, such as ovipositor size (insects) or pelvic aperture width (lizards and turtles), limit egg size. Egg size may therefore increase with female body size due to body size‐specific constraints on investment per offspring, coupled with selection towards an optimal egg size. We use 17 years of data from a population of painted turtles Chrysemys picta to evaluate this hypothesis. In accordance with our predictions, we find that (1) morphological constraints on egg size are apparent only in relatively small females, similarly (2) egg mass exhibits a strong asymptotic relationship with female body size, suggesting egg mass is optimized only at large body sizes, (3) clutch size, not egg mass, varies with female condition, and (4) clutch size varies more than egg mass across years. Contrary to our predictions, we observe that (5) the egg mass‐clutch size tradeoff is not less pronounced at large body sizes. Our data do not fully support the traditional hypothesis, and recent models suggest that this hypothesis is indeed overly simplistic. When the selective environment of a female's offspring is influenced by her phenotype, optimal egg size may vary among maternal phenotypes. This concept can explain correlations among egg size and body size in many taxa, as well as the patterns observed in the present study. In this paradigm, a tight coupling of aperture width (or other ‘constraints’) and egg size may occur in small females, even when such morphological features are not causally related to variation in egg size. In this spirit, we question validity of invoking morphological constraints to explain covariation among egg size and female body size.     

Maternal age and egg weight affect offspring performance in the predatory stink bug Podisus nigrispinus

To investigate influences of maternal age and egg weight on developmental time and body weight of offspring in the Neotropical pentatomid Podisus nigrispinus, a study was carried out using large (0.36 mg) and small (0.32 mg) eggs of young (two-week- old) females and large eggs of old (seven-week-old) females. Incubation period of eggs was influenced only by egg weight, i.e. small eggs took a relatively shorter time to hatch. Both maternal age and egg weight had significant effects on total nymphal and egg-to- adult developmental times. Overall, offspring of young parents had shorter developmental times. None of the developmental periods were significantly affected by sex. No significant differences were found among various offspring groups for percentages of egg hatch, nymphal survival, and sex ratio. Variation of egg weight in relation to the number of eggs per day observed within the first month of life suggests a trade-off between weight of individual eggs and oviposition rate. It is concluded that for mass production of the predators in view of their use in augmentative biocontrol programmes, young parents (2–4 weeks old) should be preferred.     

How avian incubation behaviour influences egg surface temperatures: relationships with egg position,development and clutch size

While understanding heat exchange between incubating adults and their eggs is central to the study of avian incubation energetics, current theory based on thermal measurements from dummy eggs reveals little about the mechanisms of this heat exchange or behavioural implications for the incubating bird. For example, we know little about how birds distribute their eggs based on temperature differences among egg positions within the nest cup. We studied the great tit Parus major, a species with a large clutch size, to investigate surface cooling rates of individual eggs within the nest cup across a range of ambient temperatures in a field situation. Using state‐of‐the‐art portable infrared imaging and digital photography we tested for associations between egg surface temperature (and rate of cooling) and a combination of egg specific (mass, shape, laying order, position within clutch) and incubation specific (clutch size, ambient temperature, day of incubation) variables. Egg surface temperature and cooling rates were related to the position of the eggs within the nest cup, with outer eggs being initially colder and cooling quicker than central eggs. Between foraging bouts, females moved outer eggs significantly more than centrally positioned eggs. Our results demonstrate that females are capable of responding to individual egg temperature by moving eggs around the nest cup, and that the energy cost to the female may increase as incubation proceeds. In addition, our results showing that smaller clutches experience lower initial incubation temperatures and cool quicker than larger clutches warrant further attention for optimal clutch size theory and studies of energetic constraints during incubation. Finally, researchers using dummy eggs to record egg temperature have ignored important elements of contact‐incubation, namely the complexity of how eggs cool and how females respond to these changes.     

Factors affecting egg maturation in the bean weevil Callosobruchus maculatus

Abstract. This paper concerns the effects of mate and seed availability on the rate of egg maturation in the bean weevil Callosobruchus maculatus (F.). Egg maturation starts before emergence from the seed and, provided that both oviposition sites and mates are available, eggs are laid at a rate determined by the number of oviposition sites, and mature at a similar rate. If seeds or mates are absent then a small number of eggs are laid, but oocytes continue to mature until the oviduct-capacity is approached. The number of eggs that a female can store is dependent on her body weight and does not correlate with the number of ovarioles. If, after a period in which oocyte development has been halted, conditions for egg-laying become suitable, then egg maturation can be re-started, but only after the oviducts have been emptied of eggs. The rate of egg maturation is then similar to that for females of the same age which have been maturing eggs since emergence.     

Elevated corticosterone during egg production elicits increased maternal investment and promotes nestling growth in a wild songbird

Glucocorticoids circulating in breeding birds during egg production accumulate within eggs, and may provide a potent form of maternal effect on offspring phenotype. However, whether these steroids affect offspring development remains unclear. Here, we employed a non-invasive technique that experimentally elevated the maternal transfer of corticosterone to eggs in a wild population of house wrens. Feeding corticosterone-injected mealworms to free-living females prior to and during egg production increased the number of eggs that females produced and increased corticosterone concentrations in egg yolks. This treatment also resulted in an increase in the amount of yolk allocated to eggs. Offspring hatching from these eggs begged for food at a higher rate than control offspring and eventually attained increased prefledging body condition, a trait predictive of their probability of recruitment as breeding adults in the study population. Our results indicate that an increase in maternal glucocorticoids within the physiological range can enhance maternal investment and offspring development.