Ontogenic sources of variation in sexual size dimorphism in a viviparous lizard

To elucidate the developmental aspects of the evolution of sexual size dimorphism (SSD), an understanding of the sex-specific ontogeny of body size is critical. Here, we evaluate the relative importance of genetic and environmental determinants of SSD in juvenile common lizards (Lacerta vivipara). We examined the prenatal and post-natal effects of population density and habitat humidity on SSD, as well as the maternal effects of food availability, corticosterone level, humidity and heat regime during gestation. Analyses indicated strong prenatal and post-natal plasticity in body size per se and yielded three main results with respect to SSD. First, SSD in juvenile common lizards matches qualitatively the SSD observed in adults. Secondly, SSD was influenced by none of the prenatal factors investigated here, suggesting poor sex-biased maternal effects on offspring size. Thirdly, SSD was sensitive to post-natal habitat humidity, which positively affected growth rate more strongly in females than in males. Thus, natural variation in SSD in juvenile common lizards appears to be primarily determined by a combination of sex-biased genetic factors and post-natal conditions. We discuss the possibility that viviparity may constrain the evolution of sex-biased maternal effects on offspring size.     

Experimental evidence of early costs of reproduction in conspecific viviparous and oviparous lizards

Reproduction entails costs, and disentangling the relative importance of each stage of the reproductive cycle may be important to assess the costs and benefits of different reproductive strategies. We studied the early costs of reproduction in oviparous and viviparous lizard females of the bimodal reproductive species Zootoca vivipara. Egg retention time in oviparous females is approximately one-third of the time in viviparous females. We compared the vitellogenesis and egg retention stages that are common to both reproductive modes. Precisely, we monitored the thermoregulatory behaviour, the weight gain and the immunocompetence of the females. Moreover, we injected an antigen in half of the females (immune challenge) to study the trade-offs between reproductive mode and immune performance and between different components of the immune system. Finally, we experimentally induced parturition in viviparous females at the time of egg laying in oviparous females. Oviparous and viviparous females did not show strong differences in response to the immune challenge. However, viviparous females spent more time thermoregulating while partially hidden and gained more weight than oviparous females. The greater weight gain indicates that the initial period of egg retention is less costly for viviparous than for oviparous females or that viviparous females are able to save and accumulate energy at this period. This energy may be used by viviparous females to cope with the subsequent costs of the last two-third of the gestation. Such an ability to compensate the higher costs of a longer egg retention period may account for the frequent evolution of viviparity in squamate reptiles.     

Manipulating developmental stress reveals sex-specific effects of egg size on offspring phenotype

The general lack of experimental evidence for strong, positive effects of egg size on offspring phenotype has led to suggestions that avian egg size is a neutral trait. To better understand the functional significance of intra-specific variation in egg size as a determinant of offspring fitness within a life-history (sex-specific life-history strategies) and an environmental (poor rearing conditions) context, we experimentally increased developmental stress (via maternal feather-clipping) in the sexually size-dimorphic European starling (Sturnus vulgaris) and measured phenotypic traits in offspring across multiple biological scales. As predicted by life-history theory, sons and daughters had different responses when faced with developmental stress and variation in egg size. In response to developmental stress, small egg size in normally faster-growing sons was associated with catch-up growth prior to attaining larger adult size, resulting in a reduction in developmental stability. Daughters apparently avoided this developmental instability by reducing growth rate and eventual adult body mass and size. Interestingly, large egg size provided offspring with greater developmental flexibility under poor growth conditions. Large-egg sons and daughters avoided the reduction in developmental stability, and daughters also showed enhanced escape performance during flight trials. Furthermore, large egg size resulted in elevated immune responses for both sexes under developmental stress. These findings show that there can be significant, but complex, context-specific effects of egg size on offspring phenotype at least up to fledging, but these can only be demonstrated by appreciating variation in the quality of the offspring environment and life histories. Results are therefore consistent with egg size playing a significant role in shaping the phenotypic outcome of offspring in species that show even greater intra-specific variation in egg size than starlings.     

Unit pricing: Economics and the evolution of litter size

Variability in litter size and the concept of optimality are central to our current understanding of parental investment patterns and life histories. A fundamental component of most models of optimum litter size is an apparently inescapable trade-off between litter size and size of offspring. Most previous models of litter size have focused on the evolution of an optimum litter size rather than variability in litter size. Because variability provides the raw material from which numerous optimal litter sizes are fashioned to meet prevailing conditions, approaches that specifically address adaptive patterns of variability might provide new insights into the evolution of litter size. A model based on a non-linear relationship between total parental effort and litter size reduces trade-offs between offspring size and offspring number to simple reproductive economics, and illustrates how litter size variability might be predictable under certain environmental conditions. This revised version was published online in July 2006 with corrections to the Cover Date.     

Climate effects on offspring sex ratio in a viviparous lizard

1. Understanding individual and population responses to climate change is emerging as an important challenge. Because many phenotypic traits are sensitive to environmental conditions, directional climate change could significantly alter trait distribution within populations and may generate an evolutionary response. 2. In species with environment-dependent sex determination, climate change may lead to skewed sex ratios at hatching or birth. However, there are virtually no empirical data on the putative link between climatic parameters and sex ratios from natural populations. 3. We monitored a natural population of viviparous lizards with temperature-dependent sex determination (Niveoscincus ocellatus) over seven field seasons. Sex ratios at birth fluctuated significantly among years and closely tracked thermal conditions in the field, with the proportion of male offspring increasing in colder years. 4. This is the first study to demonstrate the effect of local climatic conditions (e.g. temperature) on offspring sex ratio fluctuations in a free-living population of a viviparous ectotherm. A succession of warmer-than-usual years (as predicted under many climate-change scenarios) likely would generate female-biased sex ratios at birth, while an increase in interannual variation (as also predicted under climate change scenarios) could lead to significant fluctuations in cohort sex ratios. If cohort sex ratio bias at birth leads to adult sex ratio bias, long-term directional changes in thermal conditions may have important effects on population dynamics in this species.     

Short- and long-term effects of litter size manipulation in a small wild-derived rodent

Iteroparous organisms maximize their overall fitness by optimizing their reproductive effort over multiple reproductive events. Hence, changes in reproductive effort are expected to have both short- and long-term consequences on parents and their offspring. In laboratory rodents, manipulation of reproductive efforts during lactation has however revealed few short-term reproductive adjustments, suggesting that female laboratory rodents express maximal rather than optimal levels of reproductive investment as observed in semelparous organisms. Using a litter size manipulation (LSM) experiment in a small wild-derived rodent (the common vole; Microtus arvalis), we show that females altered their reproductive efforts in response to LSM, with females having higher metabolic rates and showing alternative body mass dynamics when rearing an enlarged rather than reduced litter. Those differences in female reproductive effort were nonetheless insufficient to fully match their pups’ energy demand, pups being lighter at weaning in enlarged litters. Interestingly, female reproductive effort changes had long-term consequences, with females that had previously reared an enlarged litter being lighter at the birth of their subsequent litter and producing lower quality pups. We discuss the significance of using wild-derived animals in studies of reproductive effort optimization.     

Impact of the ESR gene on litter size and production traits in Czech Large White pigs

To evaluate the effect of the PvuII polymorphism of the oestrogen receptor gene on litter size and production traits in Czech Large White swine, data from 1250 sows and 3600 litters were analysed with two four-trait animal models. The traits in the first model were number of piglets born alive in a sow's first litter, number of piglets born alive in second and subsequent litters, lifetime daily gain and lean meat percentage. The second model included number of piglets born, number of piglets born alive, number of piglets weaned and litter weight at weaning from first and subsequent litters. The oestrogen receptor (ESR) locus significantly affected prolicacy in the first parity and averaged over all parities (P < 0.05), with allele A superior to allele B. In the first parity, AA sows produced approximately 0.5 more live piglets per litter than BB sows. Averaged over all parities, this difference was c. 0.25 piglets. Results for total number of piglets born and number of piglets weaned were similar to results for numbers born alive. No significant dominance effect was found for prolificacy traits. For litter weight at weaning, no significant additive effect was observed at the ESR locus, but a significant negative dominance effect (-1.5 kg) was estimated averaged across parities (litters of AB sows were similar to litters of BB sows for this trait). No pleiotropic effect of the ESR polymorphism on average daily gain or lean meat percentage was found.     

Effects of gestation temperature on offspring sex and maternal reproduction in a viviparous lizard (Eremias multiocellata) living at high altitude

Temperature-dependent sex determination (TSD) is well studied in many species of reptiles, but little is known on how geographic distribution and altitude affect the sex ratio. In the present study, we focused on a population of a viviparous lizard with TSD (Eremias multiocellata) that lives at high altitudes (≈2900 m) in Tianzhu, Gansu province, China. Gestation temperature had a notable effect on the offspring sex ratio, gestation period, and the mother's body mass. The mothers produced female biased offspring at 25 °C but male biased offspring at 35 °C. All female lizards lost weight during pregnancy, and the least loss of the body mass was observed at 31 °C. The gestation period increased in a non-linear fashion as ambient temperature was reduced. Average litter size was elevated with an increase of gestation temperatures, reached a maximum at 31 °C, and then declined at 35 °C. Compared with a previous study on a Minqin population which lives at a lower altitude (≈1400 m) and warmer climate, the present study obtained a less skewed sex ratio of offspring in the Tianzhu population. Geographic variations also affected offspring morphology between the two populations; females collected from Tianzhu produced larger litters but with a smaller body weight of offspring. These differences may be caused by the adaptive response to the cool climatic and high-altitude environmental conditions.     

Genetic parameters for canalisation analysis of litter size and litter weight traits at birth in mice

The aim of this research was to explore the genetic parameters associated with environmental variability for litter size (LS), litter weight (LW) and mean individual birth weight (IW) in mice before canalisation. The analyses were conducted on an experimental mice population designed to reduce environmental variability for LS. The analysed database included 1976 records for LW and IW and 4129 records for LS. The total number of individuals included in the analysed pedigree was 3997. Heritabilities estimated for the traits under an initial exploratory approach varied from 0.099 to 0.101 for LS, from 0.112 to 0.148 for LW and from 0.028 to 0.033 for IW. The means of the posterior distribution of the heritability under a Bayesian approach were the following: 0.10 (LS), 0.13 (LW) and 0.03 (IW). In general, the heritabilities estimated under the initial exploratory approach for the environmental variability of the analysed traits were low. Genetic correlations estimated between the trait and its variability reached values of -0.929 (LS), -0.815 (LW) and 0.969 (IW). The results presented here for the first time in mice may suggest a genetic basis for variability of the evaluated traits, thus opening the possibility to be implemented in selection schemes.     

Effect of gestation temperature on sexual and morphological phenotypes of offspring in a viviparous lizard, Eremias multiocellata

It has been documented in some reptiles that thermal environment can induce variation in sex ratio and morphological phenotypes of offspring. Here, the viviparous lizards (Eremias multiocellata) were maintained under different temperatures during pregnancy to test the effects of this treatment on sexual and morphological phenotypes of offspring, and to investigate whether this lizard is subject to temperature-dependent sex determination (TSD). The warmer temperatures resulted in shorter gestation periods and a higher ratio of male: female births; however, gestation temperature did not affect the neonates’ body mass or snout–vent length (SVL). The gestation temperatures also had significant effects on the mean litter size. Therefore, our results show that the viviparous lizard E. multiocellata might be a TSD species, providing the mothers the opportunity to manipulate the sex ratio of their offspring.     

Analysis of the oviductal glycoprotein 1 polymorphisms and their effects on components of litter size in rabbits

The objective of this work was to study the effect of the oviductal glycoprotein 1 ( OVGP1 ) genotype and mRNA expression on litter size and other fertility measures, as OVGP1 has positive effects on fertilization and early embryo development. We have analysed an F₂ cross of two lines of rabbits divergently selected for uterine capacity. The OVGP1 mRNA expression was analysed in both lines, but no differences were observed between them. The promoter region and mRNA were sequenced in the F₀ generation, and 17 polymorphic sites were found to co-segregate in three haplotypes (A, B and C). An association study was performed between several reproductive traits and a triallelic microsatellite identified in the promoter region as well as a non-synonymous SNP located in exon 11 [g.12944C>G (p.Arg468Gly)]. The alleles g.12944G and g.325(GT)₁₄T(G)₅ of the B haplotype have a positive effect on the total number of kits born, number born alive, number of implanted embryos and foetal and prenatal embryo survival.     

Relationships between oviposition date, hatch date, and offspring size in the grasshopper Chorthippus brunneus

Abstract 1. The grasshopper Chorthippus brunneus has been shown to increase egg size with maternal age under constant laboratory conditions, such that late-laid eggs are larger than early laid eggs. In this study, an increase in the size of eggs (and hatchlings from those eggs) was recorded with date of oviposition in a field cage population. This suggests that the relationship between maternal age and egg size, observed previously in the laboratory, also occurs in the field. There was, however, some evidence that the behaviour of the maternal females in field cages was modified by the onset of autumnal weather at the end of the breeding season. Only a small number of eggs was laid in the last 3 weeks of the summer but these yielded relatively small hatchlings.
2. The date on which eggs were laid was correlated positively with their date of hatch in the following year. A consequence of this relationship, and that between oviposition date and egg size, was that size at hatch increased with date of hatch through most of the spring but then declined as the last few eggs hatched. Temporal variation in size at hatch parallelled temporal variation in the maternal females' investment in egg size in the previous year.
3. An undisturbed field population was monitored to assess whether the temporal variation in size at hatch resulted in size variation at eclosion in subsequent developmental stages. There were negative correlations between size at eclosion and date of eclosion at the third and fourth instars, suggesting that despite their smaller size at hatch, early hatchers experienced more favourable conditions for juvenile growth than late hatchers. The larger size at hatch of late hatchers may enhance their survival and compensate (albeit incompletely) for their reduced opportunity for growth. Female reproductive behaviour may represent an adaptive response to a predictable seasonal decline in offspring fitness at hatch.     

Reproductive allocation and the long-term costs of reproduction in Siparuna grandiflora, a dioecious neo-tropical shrub

1 Using a combination of observational and experimental approaches, both allocation of resources to reproduction (often called the direct cost of reproduction) and the subsequent long-term costs (the indirect, delayed or demographic cost) associated with reproductive allocation to male and female function in Siparuna grandiflora (Siparunaceae), a tropical dioecious shrub, were examined.
2 The objectives were to determine whether females allocate more biomass or nitrogen per reproductive episode than males, and whether there is a long-term cost of reproduction in terms of subsequent growth or reproduction for either sex. If there is no long-term cost of reproduction, then reproduction may be viewed as free in an evolutionary sense.
3 As is generally the case in dioecious species, females allocated more biomass and nitrogen to reproduction than males. Females also showed delayed costs of reproduction in terms of decreased growth and subsequent reproduction, whereas males did not.
4 The lack of measurable delayed costs in males suggests that with the evolution of dioecy, selection has reduced delayed costs of reproduction in S. grandiflora males. In contrast, females that were prevented from reproducing were able to re-allocate resources to growth, and produced more stem length on average than males. This re-allocation response may have evolved to reduce delayed costs of reproduction in females over time frames longer than that considered in the present study.     

The causes and consequences of variation in offspring size: a case study using Daphnia

Offspring size can have large and direct fitness implications, but we still do not have a complete understanding of what causes offspring size to vary. Daphnia (water fleas) generally produce fewer and larger offspring when food is limited. Here, we use a mathematical model to show that this could be explained by either: (1) an advantage of producing larger eggs when food is limited; or (2) a lower boundary on egg volume (below which eggs do not have sufficient resources to be viable), that is similar in volume to the evolutionarily stable egg volume predicted by standard clutch size models. We tested the first possibilities experimentally by placing offspring from mothers kept at two food treatments (high and low - leading to relatively small and large eggs respectively) into two food treatments (same as maternal treatments, in a fully factorial design) and measuring their fitness (reproduction, age at maturity, and size at maturity). We also tested survival under starvation conditions of offspring produced from mothers at low and high food treatments. We found that (larger) offspring produced by low-food mothers actually had lower fitness as they took longer to reproduce, regardless of their current food treatment. Additionally, we found no survival advantage to being born of a food-stressed mother. Consequently, our results do not support the hypothesis that there is an advantage to producing larger eggs when food is limited. In contrast, data from the literature support the importance of a lower boundary on egg size.