Evidence for the morphological constraint hypothesis and optimal offspring size theory in the Mexican mud turtle (Kinosternon integrum)

Optimal offspring size theory states that natural selection should balance reproductive output by optimizing between offspring size and offspring number. If a species has evolved an optimal offspring size, the fitness of larger females should be increased by simply producing more offspring of an optimum size. In contrast, when offspring size is not optimized, the morphological constraint hypothesis may apply, and in this case, maternal fitness is increased by producing the greatest number of the largest offspring that mothers are physically capable of producing. We used a log-log allometric regression approach on clutch size, egg size, and body size data to test the application of optimal offspring size theory and the morphological constraint hypothesis in the Mexican mud turtle (Kinosternon integrum) in southern Mexico. Our results indicate that this turtle seems to follow the morphological constraint hypothesis when all data are analyzed together, but when data are divided between small (< 140 mm plastron length) and large females (> 140 mm plastron length), optimal offspring (egg) size theory was supported only in large females, while the morphological constraint hypothesis was supported in small females. Our results thus indicate that K. integrum females may increase their fitness in two different, size-dependent ways as they grow from size at sexual maturity to maximum body size.     

A new look at relationships between size at maturity and asymptotic size

Comparative studies have revealed positive correlations between size at maturity and asymptotic size in several taxa with asymptotic growth after maturity. Using a simple growth model, we show that positive correlations between size at maturity and asymptotic size are predicted for different individuals in the same species if growth costs of reproduction are inversely related to size at maturity. Several processes might lead to higher growth costs of reproduction for smaller individuals; these include effects of body size on competition for resources required for breeding, on the space available within the body cavity for food processing in gravid individuals, and on the costs of transporting eggs or young in relation to the total energy budget. We confirm several key elements of the growth model using data from female Iguana iguana lizards, including the novel assumption that instantaneous growth rates of adults of the same length will be positively related to their length at maturity. These analyses suggest a simple and possibly general explanation for positive correlations between size at maturity and asymptotic size within-and perhaps also among-species that continue to grow after maturity.     

Offspring size and timing of hatching determine survival and reproductive output in a lizard

Selection on offspring size and timing of birth or hatching could have important consequences for maternal investment strategies. Here we show consistent viability selection on hatchling body length across 2 consecutive years in a lizard that lays several clutches per season. There was no effect of hatching date on survival to maturity. However, both early hatching and large hatchling size increased adult size, which has a positive effect on total reproductive output. Earlier hatching also led to an earlier onset of reproduction. Overall, increased survival probability for large hatchlings and a positive effect of clutch size on recruitment suggest consistent directional selection on both egg size and clutch size within and across years. Because offspring size and timing of hatching are strongly affected by environmental and maternal effects, there should be potential for strong transgenerational effects on reproductive output in this species. We briefly discuss the implications of these results for the evolutionary ecology of maternal investment and population fluctuations in short-lived lizards.     

Does the differential cost of sons and daughters lead to sex ratio adjustment in great frigatebirds Fregataminor?

Sex allocation theory predicts that if benefits of producing sons and daughters differ and outweigh the costs of sex ratio adjustment, parents should produce more of the offspring that provide them with greater fitness. Potential benefits may be more likely to outweigh costs where sexual size dimorphism and, in birds, single‐egg clutches exist. Great frigatebirds Fregataminor are seabirds in which females are larger than males and clutch size is one egg. In our study population, sexual size dimorphism develops primarily during the period of complete juvenile dependence on parental care, consistent with a higher cost of producing daughters than sons. Over the course of the 1998 breeding season there was a shift from early season prevalence of daughters to late‐season prevalence of sons. Variation in food availability at time of egg laying, as indexed by sea surface temperature (SST), was a strong predictor of offspring sex in 1998. In contrast, SST in 2003 was not a predictor of offspring sex, nor was there a seasonal shift in the hatching sex ratio, despite a seasonal shift in SST. Besides food availability, we tested two additional factors in 2003 that could explain sex ratio adjustment in relation to the cost of reproduction. Offspring sex in 2003 was not related to natural or experimentally induced variation in maternal body condition; pre‐laying food supplements raised the body condition of females at the time of egg laying but did not affect offspring sex or egg mass. In addition, offspring sex was not predicted by the length of maternal telomere restriction fragments (TRFs), an index of age and possibly of reproductive experience. Broad confidence intervals on effect size suggest that undetected effects of maternal condition on offspring sex ratio could easily exist, but confidence intervals were narrower on the non‐significant effects of SST and TRF length on offspring sex ratio. The cause of different seasonal patterns of hatching sex ratio and different SST effects in 1998 and 2003 is unclear.     

INTERACTIVE EFFECTS OF OFFSPRING SIZE AND TIMING OF REPRODUCTION ON OFFSPRING REPRODUCTION: EXPERIMENTAL,MATERNAL, AND QUANTITATIVE GENETIC ASPECTS

We demonstrate that egg size in side-blotched lizards is heritable (parent-offspring regressions) and thus will respond to natural selection. Because our estimate of heritability is derived from free-ranging lizards, it is useful for predicting evolutionary response to selection in wild populations. Moreover, our estimate for the heritability of egg size is not likely to be confounded by nongenetic maternal effects that might arise from egg size per se because we estimate a significant parent-offspring correlation for egg size in the face of dramatic experimental manipulation of yolk volume of the egg. Furthermore, we also demonstrate a significant correlation between egg size of the female parent and clutch size of her offspring. Because this correlation is not related to experimentally induced maternal effects, we suggest that it is indicative of a genetic correlation between egg size and clutch size. We synthesize our results from genetic analyses of the trade-off between egg size and clutch size with previously published experiments that document the mechanistic basis of this trade-off. Experimental manipulation of yolk volume has no effect on offspring reproductive traits such as egg size, clutch size, size at maturity, or oviposition date. However, egg size was related to offspring survival during adult phases of the life history. We partitioned survival of offspring during the adult phase of the life history into (1) survival of offspring from winter emergence to the production of the first clutch (i.e., the vitellogenic phase of the first clutch), and (2) survival of the offspring from the production of the first clutch to the end of the reproductive season. Offspring from the first clutch of the reproductive season in the previous year had higher survival during vitellogenesis of their first clutch if these offspring came from small eggs. We did not observe selection during these prelaying phases of adulthood for offspring from later clutches. However, we did find that later clutch offspring from large eggs had the highest survival over the first season of reproduction. The differences in selection on adult survival arising from maternal effects would reinforce previously documented selection that favors the production of small offspring early in the season and large offspring later in the season—a seasonal shift in maternal provisioning. We also report on a significant parent-offspring correlation in lay date and thus significant heritable variation in lay date. We can rule out the possibility of yolk volume as a confounding maternal effect—experimental manipulation of yolk volume has no effect on lay date of offspring. However, we cannot distinguish between genetic effects (i.e., heritable) and nongenetic maternal effects acting on lay date that arise from the maternal trait lay date per se (or other unidentified maternal traits). Nevertheless, we demonstrate how the timing of female reproduction (e.g., date of oviposition and date of hatching) affect reproductive attributes of offspring. Notably, we find that date of hatching has effects on body size at maturity and fecundity of offspring from later clutches. We did not detect comparable effects of lay date on offspring from the first clutch.     

The trade-off between number and size of offspring in humans and other primates

Life-history theory posits a fundamental trade-off between number and size of offspring that structures the variability in parental investment across and within species. We investigate this 'quantity-quality' trade-off across primates and present evidence that a similar trade-off is also found across natural-fertility human societies. Restating the classic Smith-Fretwell model in terms of allometric scaling of resource supply and offspring investment predicts an inverse scaling relation between birth rate and offspring size and a (-1/4) power scaling between birth rate and body size. We show that these theoretically predicted relationships, in particular the inverse scaling between number and size of offspring, tend to hold across increasingly finer scales of analyses (i.e. from mammals to primates to apes to humans). The advantage of this approach is that the quantity-quality trade-off in humans is placed into a general framework of parental investment that follows directly from first principles of energetic allocation.     

SEVERE COSTS OF REPRODUCTION PERSIST IN ANOLIS LIZARDS DESPITE THE EVOLUTION OF A SINGLE‐EGG CLUTCH

A central tenet of life‐history theory is that investment in reproduction compromises survival. We tested for costs of reproduction in wild brown anoles (Anolis sagrei) by eliminating reproductive investment via surgical ovariectomy and/or removal of oviductal eggs. Anoles are unusual among lizards in that females lay single‐egg clutches at frequent intervals throughout a lengthy reproductive season. This evolutionary reduction in clutch size is thought to decrease the physical burden of reproduction, but our results show that even a single egg significantly impairs stamina and sprint speed. Reproductive females also suffered a reduction in growth, suggesting that the cumulative energetic cost of successive clutches constrains the allocation of energy to other important functions. Finally, in each of two separate years, elimination of reproductive investment increased breeding‐season survival by 56%, overwinter survival by 96%, and interannual survival by 200% relative to reproductive controls. This extreme fitness cost of reproduction may reflect a combination of intrinsic (i.e., reduced allocation of energy to maintenance) and extrinsic (i.e., increased susceptibility to predators) sources of mortality. Our results provide clear experimental support for a central tenet of life‐history theory and show that costs of reproduction persist in anoles despite the evolution of a single‐egg clutch.     

Relationships of maternal body size and morphology with egg and clutch size in the diamondback terrapin,Malaclemys terrapin (Testudines: Emydidae)

Because resources are finite, female animals face trade‐offs between the size and number of offspring they are able to produce during a single reproductive event. Optimal egg size (OES) theory predicts that any increase in resources allocated to reproduction should increase clutch size with minimal effects on egg size. Variations of OES predict that egg size should be optimized, although not necessarily constant across a population, because optimality is contingent on maternal phenotypes, such as body size and morphology, and recent environmental conditions. We examined the relationships among body size variables (pelvic aperture width, caudal gap height, and plastron length), clutch size, and egg width of diamondback terrapins from separate but proximate populations at Kiawah Island and Edisto Island, South Carolina. We found that terrapins do not meet some of the predictions of OES theory. Both populations exhibited greater variation in egg size among clutches than within, suggesting an absence of optimization except as it may relate to phenotype/habitat matching. We found that egg size appeared to be constrained by more than just pelvic aperture width in Kiawah terrapins but not in the Edisto population. Terrapins at Edisto appeared to exhibit osteokinesis in the caudal region of their shells, which may aid in the oviposition of large eggs.     

Offspring size at weaning affects survival to recruitment and reproductive performance of primiparous gray seals

Offspring size affects survival and subsequent reproduction in many organisms. However, studies of offspring size in large mammals are often limited to effects on juveniles because of the difficulty of following individuals to maturity. We used data from a long‐term study of individually marked gray seals (Halichoerus grypus; Fabricius, 1791) to test the hypothesis that larger offspring have higher survival to recruitment and are larger and more successful primiparous mothers than smaller offspring. Between 1998 and 2002, 1182 newly weaned female pups were branded with unique permanent marks on Sable Island, Canada. Each year through 2012, all branded females returning to the breeding colony were identified in weekly censuses and a subset were captured and measured. Females that survived were significantly longer offspring than those not sighted, indicating size‐selective mortality between weaning and recruitment. The probability of female survival to recruitment varied among cohorts and increased nonlinearly with body mass at weaning. Beyond 51.5 kg (mean population weaning mass) weaning mass did not influence the probability of survival. The probability of female survival to recruitment increased monotonically with body length at weaning. Body length at primiparity was positively related to her body length and mass at weaning. Three‐day postpartum mass (proxy for birth mass) of firstborn pups was also positively related to body length of females when they were weaned. However, females that were longer or heavier when they were weaned did not wean heavier firstborn offspring.     

A trade-off between current and future sex allocation revealed by maternal energy budget in a small mammal

Sex-allocation theories generally assume differential fitness costs of raising sons and daughters. Yet, experimental confirmation of such costs is scarce and potential mechanisms are rarely addressed. While the most universal measure of physiological costs is energy expenditure, only one study has related the maternal energy budget to experimentally controlled offspring sex. Here, we experimentally test this in the bank vole (Myodes glareolus) by simultaneously manipulating the litter's size and sex ratio immediately after birth. Two weeks after manipulation, when mothers were at the peak of lactation and were pregnant with concurrent litters, we assessed their energy budget. We found that maternal food consumption and daily energy expenditure increased with the size of the litters being lactated. Importantly, the effects of offspring sex on energy budget depended on the characteristics of the simultaneously gestating litters. Specifically, the mothers nursing all-male litters and concurrently pregnant with male-biased litters had the highest energy expenditure. These had consequences for the next generation, as size of female offspring from the concurrent pregnancy of these mothers was compromised. Our study attests a higher cost of sons, consequently leading to a lower investment in them, and reveals the significance of offspring sex in moulding the trade-off between current and future maternal investment.     

Experimental litter size reduction reveals costs of gestation and delayed effects on offspring in a viviparous lizard

Experimental studies have often been employed to study costs of reproduction, but rarely to study costs of gestation. Disentangling the relative importance of each stage of the reproductive cycle should help to assess the costs and benefits of different reproductive strategies. To that end, we experimentally reduced litter size during gestation in a viviparous lizard. We measured physiological and behavioural parameters during gestation and shortly after parturition, as well as survival and growth of females and their offspring. This study showed four major results. First, the experimental litter size reduction did not significantly affect the cellular immune response, the metabolism and the survival of adult females. Second, females with reduced litter size decreased their basking time. Third, these females also had an increased postpartum body condition. As postpartum body condition is positively related to future reproduction, this result indicates a gestation cost. Fourth, even though offspring from experimentally reduced litters had similar weight and size at birth as other offspring, their growth rate after birth was significantly increased. This shows the existence of a maternal effect during gestation with delayed consequences. This experimental study demonstrates that there are some costs to gestation, but it also suggests that some classical trade-offs associated with reproduction may not be explained by gestation costs.     

Ovarian maturity,egg development,and offspring generation of the deep-water shrimp Plesionika edwardsii (Decapoda,Pandalidae) from three isolated populations in the eastern North Atlantic

Ovarian maturity, egg development and brood size were analysed for three isolated populations (Madeira, the Canary Islands and Cape Verde Islands) of Plesionika edwardsii (Decapoda, Pandalidae) in the eastern Atlantic. Multiple colour patterns were observed at the same ovarian maturity stage, which was verified histologically, invalidating the extensive use of ovarian colour as a maturity stage criterion. The physiological size at sexual maturity, based on the maturity of the ovaries, was higher in Madeira (carapace length of 19.73?mm) and decreased to the Cape Verdes (16.39?mm). Synchronic ovarian maturation was observed during the embryo incubation process, and ovigerous females bearing embryos at the final stage of development were found throughout the year. Females are multiple spawners during the reproductive season, after which the reproductive process ends and a rest period begins. The absence of females larger than the size at sexual maturity with ovaries in Stage 1, the incubation of embryos in the final developmental stages, suggests that the resting period begins with a process that reabsorbs the energy located in the ovaries and that the resting period occurs asynchronously in females in each of the studied populations. Embryo size was independent of female body size in the three populations studied, but increased with the developmental stage. A power equation was used to describe the relationship between brood size and female body size in the three areas studied. The mean number of external Stage I embryos carried by females decreased from Madeira (n?=?7868) to the Cape Verdes (n?=?3781), where less energy, in terms of the number of embryos and the size of the eggs, was invested in reproduction. Although female size decreases from north to south, the egg number was higher in Madeira than in the Cape Verdes for the same size range.     

Egg size evolution and energetic constraints on population dynamics.

We use population models that are based on dynamic energy budget models for individuals in order to study the evolution of offspring size and its relationship to the evolution of population dynamics. We show the existence of alternative evolutionarily stable strategies for offspring investment strategy resulting from a trade off between offspring number and time-to-maturity. The model predicts egg energy in Daphnia magna well, and suggests that the observed egg energy in D. magna is the result of selection for minimal egg investment constrained by minimum viable egg energy, combined with selection for a juvenile energy reserve. The selection for minimal egg size pushes populations toward chaotic dynamics. However, the minimum viable egg size combined with low efficiency of conversion of energy to new biomass is sufficient to keep population dynamics out of chaos.     

On the virtue of being the first born: the influence of date of birth on fitness in the mosquitofish, Gambusia affinis

We found in an earlier study that mosquitofish (Gambusia affinis and G. holbrooki) ceased reproduction in the late summer, long before the end of warm weather, stored fat, then utilized reserves to survive the winter and initiate reproduction the following spring. We hypothesized that this pattern of fat utilization was a life history adaptation that enabled the fish to acquire food resources in the autumn then allocate them to reproduction the following spring when the fitness of the young would be greater. Here we evaluate one aspect of this hypothesis by evaluating the probability of survival to maturity and fecundity of young as a function of date of birth. We placed cohorts comprising eight to ten litters of young born early‐, mid‐ or late in the reproductive season in replicate field enclosures. The entire experiment was repeated in two different years. Early‐born young had a significantly higher probability of survival to maturity but did not differ in fecundity relative to the last cohort of the season. Early‐born young also attained maturity early enough to reproduce in their year of birth while late‐born young had to overwinter before reproduction. The fitness consequences to the mother of either producing one more litter of young at the end of the season, versus instead storing fat and reproducing the following spring are not as determinate as are the effects of date of birth on offspring fitness. Females most often gain fitness by not producing one last litter and instead over‐wintering. If, however, the overwinter survival of offspring is not influenced by their size at the end of the season, then a female's fitness could be enhanced by producing one more litter late in the season. If instead the probability of overwinter survival is strongly influenced by the size of offspring at the end of the season, then our results suggest that a female gains more by deferring reproduction and storing for overwinter survival and reproduction the following spring.     

A Review for Life-history Traits Variation in Frogs Especially for Anurans in China

Environmental variation can promote differentiation in life-history traits in species of anurans. Increased environmental stress usually results in larger age at sexual maturity, older mean age, longer longevity, slower growth, larger body size, and a shift in reproductive allocation from offspring quantity to quality, and a stronger trade-off between offspring size and number. However, previous studies have suggested that there are inconsistent geographical variations in life-history traits among anuran species in China. Hence, we here review the intraspecific patterns and differences in life-history traits(i.e., egg size, clutch size, testes size, sperm length, age at sexual maturity, longevity, body size and sexual size dimorphism) among different populations within species along geographical gradients for anurans in China in recent years. We also provide future directions for studying difference in sperm performance between longer and shorter sperm within a species through transplant experiments and the relationships between metabolic rate and brain size and life-history.     

The cost of reproduction induced by body size at birth and breeding density

Body size at birth has implications for the quality of individuals throughout their life. Although large body size is generally considered an advantage, the relationship between body size at birth and long-term fitness is often complicated. Under spatial or temporal variation in environmental conditions, such as the seasonally changing densities of Fennoscandian vole populations, selection should favor variation in offspring phenotypes, as different qualities may be beneficial in different conditions. We performed an experiment in which a novel hormonal manipulation method was used to increase phenotypic variance in body size at birth in the bank vole (Myodes glareolus). The effects of body size on the future fitness of young males and females were then studied at varying population densities in outdoor enclosures. Our results show that small body size at birth and high breeding density increase the survival costs of reproduction. However, there was no interaction between the effects of body size and density on survival, which suggests that the fitness effects of body size were strong enough to persist under environmental variation. Moreover, litter size and the probability of breeding were more sensitive to variation in breeding density than offspring size. Therefore, it is unlikely that individual fitness could be optimized by adjusting offspring body size to the prevailing population density through adaptive maternal effects. Our results highlight the significance of the costs of reproduction in the evolution of life-history traits, and give strong experimental support for the long-term fitness effects of body size at birth.     

Effects of maternal age on reproductive traits and fitness components of the offspring in the bruchid beetle, Callosobruchus chinensis (Coleoptera: Bruchidae)

In many insect species, the size and number of eggs decrease with maternal age. Thus, both the size and number of eggs must be considered to know the exact cost of reproduction with maternal age. The resource depletion hypothesis was examined in the bruchid beetle Callosobruchus chinensis. The hypothesis explains why the egg size decreases with maternal age based on the decline of the female's reproductive capacity. A decrease was found in reproductive effort (= egg size × the number of eggs) and the fitness component of offspring with maternal age. The effects of the female's nutritional status on the relationship between maternal age and the reproductive effort of females with and without food and water were also examined. The results indicate that the decrease in size and number of eggs with maternal age can be explained by the resource depletion hypothesis in C. chinensis.     

Energetics of age-specific reproductive effort in female Harp seals, Phoca groenlandica

The theory of reproductive effort is commonly viewed in the perspective of the cost of offspring to the parent. This interpretation predicts that older females make a greater reproductive effort than younger females, for whom the cost of lost future offspring is less. The benefit early-born offspring represent in future generations is greater than that of late-born offspring in most natural populations, so, alternatively, young females should make a greater reproductive effort. These hypotheses were investigated in nursing Harp seals by examining age-specific reproductive effort in terms of energetic maternal investment.
Younger Harp seal females lost weight at the same rate as did older females. Moreover. since younger, growing females tended to start lactation with less blubber than older females. weight loss during 10 days (d) of lactation represented a greater proportion of stored energy for young females. A successfully weaned pup, therefore, constituted a greater reproductive effort for them than for older females, consistent with benefit–oriented predictions from theory.
A model is presented to outline the components of an annual energy budget for female Harp seals in the context of reproductive effort. This model indicates that young females may devote a greater proportion of their annual net energy to reproduction and take a greater risk of lost future reproduction. It also identifies areas of inadequacy of existing data on pinniped energy budgets.     

Life history patterns of a livebearing fish in contrasting environments

Summary The population dynamics and energy allocations of the Gila topminnow, a small livebearing fish, were studied in two contrasting environments, a spring run of constant characteristics and a fluctuating desert wash. Topminnows grew and matured in two basic patterns. First, many fish in both areas matured the year after their birth. Second, spring fish born early in the breeding season grew rapidly, bred within five months, and died by eight months of age. Although spring fish assimilated more energy, wash fish actually expended more calories for growth and reproduction, partly because of lower maintenance costs. Reproductive effort of long-lived spring fish varied with age between 3.1 and 6.5%; whereas efforts of short-lived spring and wash fish increased steadily with age to 5.2 and 9.8%, respectively. Although spring fish produced eggs of higher energy content, females in both areas varied their investment per offspring, apparently tracking seasonal changes in the availability of food for fry. When long-lived spring fish experienced food shortage, they allocated less energy to both growth and reproduction; in contrast, wash and short-lived spring fish under similar conditions reduced only their growth allocation. The reproductive mass in spring fish appeared to be limited by food availability, incompletely filled the abdominal space, and reflected no tradeoff between fecundity and investment per offspring. Reproduction by wash fish appeared to be limited by body space and was characterized by a tradeoff between fecundity and egg size.     

Maturity, mating and age-specific reproductive effort of the snake Natrix maura

The ecology of reproduction was studied in the snake Natrix maura. The presence of sperm in cloacal fluid was used to show the size at maturity, the season of mating and, together with information on the persistence of sperm in cloacal fluid of females after mating, the frequency of mating. These results suggest that each female mated several times per year. Female N. maura grew substantially after maturity, and clutch size increased with body size. Current and expected future reproduction increased in parallel during the period of growth after maturity; subsequently they were constant. This pattern would be expected to lead to a constant proportional allocation of energy to current reproduction. Reproductive effort (eggs/body energy) was independent of age as measured by growth rings. There was some evidence that not all stored energy was used in reproduction in the current season even when some follicles regressed.