Measuring temporal variation in reproductive output reveals optimal resource allocation to reproduction in the northern grass lizard, Takydromus septentrionalis

We measured the reproductive output of Takydromus septentrionalis collected over 5 years between 1997 and 2005 to test the hypothesis that reproductive females should allocate an optimal fraction of accessible resources in a particular clutch and to individual eggs. Females laid 1–7 clutches per breeding season, with large females producing more, as well as larger clutches, than did small females. Clutch size, clutch mass, annual fecundity, and annual reproductive output were all positively related to female size (snout–vent length). Females switched from producing more, but smaller eggs in the first clutch to fewer, but larger eggs in the subsequent clutches. The mass-specific clutch mass was greater in the first clutch than in the subsequent clutches, but it did not differ among the subsequent clutches. Post-oviposition body mass, clutch size, and egg size showed differing degrees of annual variation, but clutch mass of either the first or the second clutch remained unchanged across the sampling years. The regression line describing the size–number trade-off was higher in the subsequent clutch than in the first clutch, but neither the line for first clutch, nor the line for the second clutch varied among years. Reproduction retarded growth more markedly in small females than in large ones. Our data show that: (1) trade-offs between size and number of eggs and between reproduction and growth (and thus, future reproduction) are evident in T. septentrionalis ; (2) females allocate an optimal fraction of accessible resources in current reproduction and to individual eggs; and (3) seasonal shifts in reproductive output and egg size are determined ultimately by natural selection.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 91 , 315–324.     

The influence of maternal thermal environments on reproductive traits and hatchling traits in a Lacertid lizard,Takydromus septentrionalis

The thermal environment can induce substantial variation in important life-history traits. Experimental manipulation of the thermal environment can help researchers determine the contribution of this factor to phenotypic variation in life-history traits. During the reproductive season, we kept female northern grass lizards, Takydromus septentrionalis (Lacertidae), in three temperature-controlled rooms (25, 28 and 32 °C) to measure the effect of the maternal thermal environment on reproductive traits. Maternal thermal environment remarkably affected reproductive frequency and thereby seasonal reproductive output, but had little effect on reproductive traits per clutch or hatchling traits. Females kept at 32 °C produced more clutches and thus had shorter clutch intervals than females from 28 to 25 °C. Clutch size, clutch mass, relative clutch mass, egg size and hatchling traits did not vary among the three treatments. The eggs produced by the females were incubated at 27 °C and the traits of hatchlings were measured. The result that egg (offspring) size was independent of maternal thermal environments is consistent with the prediction of the optimal egg size (offspring) theory. The eggs produced by low temperature females (28 and 25 °C) took longer time to complete their post-oviposition development than did eggs produced by high temperature females (32 °C). This suggests that the eggs from low temperatures might have been laid when the embryos were at relatively early stages. Therefore, maternal thermal environment prior to oviposition could affect post-oviposition development in T. septentrionalis.     

Identifying sources of variation in reproductive and life-history traits among five populations of a Chinese lizard (Takydromus septentrionalis, Lacertidae)

Research on life-history traits of squamate reptiles has focused on North American species, while Asian taxa have been virtually ignored. In order to understand general patterns in reptile life histories, we need a broader data base. Our study on the slender-bodied lacertid lizard Takydromus septentrionalis provides the first detailed information on factors responsible for intraspecific variation in reproductive output and life history in a Chinese reptile. Clutches of recently collected lizards from five widely separated localities in China revealed major divergences in female body size at maturation, mean adult female body size, body condition after oviposition, size-adjusted fecundity, relative clutch mass, and mass and shape of eggs. Most of these geographical differences persisted when the same groups of females were maintained in identical conditions in captivity. Additionally, reproductive frequency during maintenance under laboratory conditions differed according to the animals' place of origin. Thus, the extensive geographical variation in reproductive and life-history traits that occurs within T. septentrionalis is exhibited even in long-term captives, suggesting that proximate factors that vary among localities (local conditions of weather and food supply) are less important determinants of life-history variation than are intrinsic (presumably genetic) influences. The maternal abdominal volume available to hold the clutch may be one such factor, based on low levels of variation in Relative Clutch Mass among populations, and geographical variation in the position of trade-off lines linking offspring size to fecundity.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 85 , 443–453.     

Repeatability and heritability of reproductive traits in free-ranging snakes

The underlying genetic basis of life-history traits in free-ranging animals is critical to the effects of selection on such traits, but logistical constraints mean that such data are rarely available. Our long-term ecological studies on free-ranging oviparous snakes (keelbacks, Tropidonophis mairii (Gray, 1841), Colubridae) on an Australian floodplain provide the first such data for any tropical reptile. All size-corrected reproductive traits (egg mass, clutch size, clutch mass and post-partum maternal mass) were moderately repeatable between pairs of clutches produced by 69 female snakes after intervals of 49-1152 days, perhaps because maternal body condition was similar between clutches. Parent-offspring regression of reproductive traits of 59 pairs of mothers and daughters revealed high heritability for egg mass (h2= 0.73, SE=0.24), whereas heritability for the other three traits was low (< 0.37). The estimated heritability of egg mass may be inflated by maternal effects such as differential allocation of yolk steroids to different-sized eggs. High heritability of egg size may be maintained (rather than eroded by stabilizing selection) because selection acts on a trait (hatchling size) that is determined by the interaction between egg size and incubation substrate rather than by egg size alone. Variation in clutch size was mainly because of environmental factors (h2=0.04), indicating that one component of the trade-off between egg size and clutch size is under much tighter genetic control than the other. Thus, the phenotypic trade-off between egg size and egg number in keelback snakes occurs because each female snake must allocate a finite amount of energy into eggs of a genetically determined size.     

Maternal investment in reproduction and its consequences in leatherback turtles

Maternal investment in reproduction by oviparous non-avian reptiles is usually limited to pre-ovipositional allocations to the number and size of eggs and clutches, thus making these species good subjects for testing hypotheses of reproductive optimality models. Because leatherback turtles (Dermochelys coriacea) stand out among oviparous amniotes by having the highest clutch frequency and producing the largest mass of eggs per reproductive season, we quantified maternal investment of 146 female leatherbacks over four nesting seasons (2001–2004) and found high inter- and intra-female variation in several reproductive characteristics. Estimated clutch frequency [coefficient of variation (CV) = 31%] and clutch size (CV = 26%) varied more among females than did egg mass (CV = 9%) and hatchling mass (CV = 7%). Moreover, clutch size had an approximately threefold higher effect on clutch mass than did egg mass. These results generally support predictions of reproductive optimality models in which species that lay several, large clutches per reproductive season should exhibit low variation in egg size and instead maximize egg number (clutch frequency and/or size). The number of hatchlings emerging per nest was positively correlated with clutch size, but fraction of eggs in a clutch yielding hatchlings (emergence success) was not correlated with clutch size and varied highly among females. In addition, seasonal fecundity and seasonal hatchling production increased with the frequency and the size of clutches (in order of effect size). Our results demonstrate that female leatherbacks exhibit high phenotypic variation in reproductive traits, possibly in response to environmental variability and/or resulting from genotypic variability within the population. Furthermore, high seasonal and lifetime fecundity of leatherbacks probably reflect compensation for high and unpredictable mortality during early life history stages in this species.     

Variation of reproductive traits in a population of the lizard Lacerta vivipara

Variation in reproductive traits (sexual maturity, clutch size, clutch weight, mean egg mass, newborn weight) was studied during a four year period in a population of the live-bearing lizard Lacerta vivipara . Sexual maturity was associated with attaining a minimum body size. Clutch size increased with female body length and litter weight increased with clutch size. A major component of the within year variation in these reproductive traits was attributable to female size. Analysis of successive clutches in individual females indicated that a significant fraction of the variation in litter size, adjusted for female length, was due to consistent differences between individuals. Newborn weight varied within and among litters, but no relations between hatchling mass or mean egg mass in a litter and other traits were detected.
Size-adjusted reproductive performances remained constant during the course of this study, even though environmental conditions (weather factors, food availability) varied annually. Observed among year variations in reproductive characteristics were attributable to differences in the body size distributions of the adult females.     

升温对北草蜥雌体繁殖、卵孵化及幼体特征的影响

在围栏条件下,比较升温和对照处理北草蜥(Takydromus septentrionalis)繁殖、卵孵化及幼体特征的差异,以揭示升温对其繁殖生活史特征的作用。升温处理对北草蜥母体体温有显著影响,但并不影响其繁殖输出。升温显著影响卵孵化期和幼体的运动能力,但不影响幼体大小等形态特征。升温条件下孵出的幼体运动能力较弱。结果表明,北草蜥母体能耐受短期的环境增温,维持相对恒定的繁殖输出;升温能影响幼体的功能表现,进而可能改变后代适合度。     

Thermal dependence of reproductive allocation in a tropical lizard

In ectotherms, environmental temperature is the most prominent abiotic factor that modulates life-history traits. We explored the influence of environmental temperature on reproduction in the Madagascar ground gecko (Paroedura picta) by measuring reproductive traits of females at constant temperatures (24, 27, 30 °C). Females of this species lay clutches of one or two eggs within short intervals. For each female, we measured egg mass for the first five clutches. For one clutch, we also measured the energetic content of eggs via bomb calorimetry. Temperature positively influenced the rate of egg production, but females at 30 °C laid smaller eggs than did females at either 24 or 27 °C. Dry mass of eggs scaled allometrically with wet mass, but this relationship was similar among thermal treatments. Females at all temperatures produced eggs with similar energy densities. Females at 24 °C allocated less energy per time unit (≈8 mW) to reproduction than did females from higher temperatures (≈12 mW). However, females at either 24 or 27 °C allocated significantly more energy per egg than did females at 30 °C. Our results demonstrate that a complex thermal sensitivity of reproductive rate can emerge from distinct thermal sensitivities of egg size, egg composition and clutch frequency.     

The population determines whether and how life-history traits vary between reproductive events in an insect with maternal care

The last reproductive event of a female is often associated with major changes in terms of both maternal and offspring life-history traits. However, the nature of these changes and the importance of population-specific environmental constraints in shaping their expression are difficult to predict and, as a consequence, poorly understood. Here, we investigated whether and how life-history traits vary between reproductive events and whether this variation is population-dependent in the European earwig Forficula auricularia. In this insect species, females produce up to two clutches during their lifetime and express extensive forms of maternal care. We conducted a common garden experiment, in which we measured 11 life-history traits of the first and second clutches of 132 females originating from three populations. Our results showed that clutch size was higher and the level of care expressed towards juveniles lower in second as compared to the first clutches in all three populations. In contrast, we found a population-specific effect on whether and how the reproductive event shaped juvenile quality and a trade-off between egg developmental time and female weight at hatching. Overall, these findings emphasise that the last reproductive event of a female entails both positive and negative effects on various life-history traits of the female herself and her clutch of juveniles. Moreover, our study stresses the importance of population idiosyncrasies on the expression and nature of such cohort-specific effects.     

Maternal androgens in the pied flycatcher: timing of breeding and within-female consistency

Maternal hormones can have substantial phenotypic effects in the progeny of many vertebrates. It has been proposed that mothers adaptively adjust hormone levels experienced by particular young to optimize their reproductive output. In birds, systematic variation in egg hormone levels has been related to different female reproductive strategies. Because in many bird species prospects of the offspring change seasonally and with brood number, strategic adjustment of yolk androgen levels would be expected. To test this idea, we induced pied flycatcher (Ficedula hypoleuca) females to nest twice during the same season by removing their first clutches shortly after clutch completion. We collected eggs of first and replacement clutches to measure yolk concentrations of androstenedione (A4) and testosterone (T) and captured the females that laid these clutches for phenotypic measurements. Although average egg androgen levels were remarkably consistent within females, hormone patterns differed considerably between first and replacement clutches. Eggs of replacement clutches were heavier with larger yolks compared to first clutches, but they contained on average lower levels of androgens. Within clutches, androgen concentration increased over the laying sequence in the first clutch, but decreased or remained more constant over the laying sequence in the replacement clutch. Mean yolk T, but not A4 levels, were negatively associated with laying date for both breeding attempts. Moreover, females in good body condition produced eggs containing lower levels of androgens than females in poor condition. Our results are consistent with the idea that differences in yolk androgen levels may be one mechanism underlying seasonal variation in reproductive success and it is possible that changes in egg androgen patterns may reflect a change in female reproductive strategy. High within-female consistency also highlights the possibility that there may be some underlying genetic variation in yolk androgen levels.     

Density effects on life-history traits of an island lizard population

Long-term monitoring of life-history traits and the effects of density upon them were studied in an island population of the lizardEumeces okadae. Although life-history traits such as clutch size, egg size and the proportion of mature reproductive females varied little over 7 years in the intact population, manipulation of density to simulate decreased population density enhanced juvenile growth rate, age at first reproduction, frequency of female reproduction and size-specific clutch mass. In particular, the proportion of mature females reproducing annually increased almost 10 times from 5.6% to 53.8% after the removal of some lizards. However, body size at first reproduction and egg size were almost identical under both high and low density conditions. This study suggests that there were strong density-dependent effects on several life-history traits and thatE. okadae attained a density close to the carrying capacity of the environment.     

Covariation in Insular Life-history Traits of the Rice Frog(Fejervarya limnocharis)in Eastern China

Although shifts in life-history traits of insular vertebrates, as compared with mainland populations, have been observed in many taxa, few studies have examined the relationships among individual life-history traits on islands. Lifehistory theory also predicts that there is a trade-off between body size and reproductive effort, and between egg size and clutch size. We surveyed the rice frog, Fejervarya limnocharis, on 20 islands within the Zhoushan Archipelago and two nearby sites on the mainland of China to compare differences in life-history traits and to explore relationships among those traits. Rice frog females reached a greater body size on half of the smaller islands among the total 20 surveyed islands, and larger egg size, decreased clutch size and reduced reproductive effort on most of the islands when compared to the two mainland sites. Insular body size was negatively correlated with reproductive effort. There was a negative correlation between egg size and clutch size. Results suggest that life-history theory provides a good explanation for co-variation between body size and reproductive effort, and between egg size and clutch size in rice frogs on the islands.     

Reproductive strategies and body shape in the European pond turtle (Emys orbicularis) from contrasting habitats in Italy

Comparisons within and among populations offer important insights into variation in life-history traits and possible adaptive patterns to environmental conditions. We present the results of observed differences in body size, body shape and patterns of reproduction in four separate populations of the European pond turtle Emys orbicularis in central and southern Italy – coastal ( n =3) and mountainous ( n =1) sites and pond ( n =2) and canal ( n= 2) habitats – to determine whether phenotypic plasticity affects reproductive output. Although we did not find any significant latitudinal variation in body size, we observed significant differences in body shape between canal (rounded body shape) and pond (elongated body shape) systems and smaller size with rounded shape in the mountainous population. Reproductive output is similar among populations (median=5 eggs per clutch), whereas reproductive investment (relative clutch mass to maternal body mass) is higher in the mountain population (one clutch per year) than in coastal populations (two clutches per year), suggesting differential trade-offs between geographic locality, elevation and habitat type. Turtle shell shape and geographic location together affect reproductive output in E. orbicularis in Italy.     

Factors affecting variation in the reproductive investment of female treefrogs,Hyla intermedia

In anurans, fecundity (clutch size) is the most important determinant of female reproductive success. We investigated three possible causes responsible for fecundity variation in female Italian treefrogs, Hyla intermedia, during four breeding seasons: (i) variation in morphological (body size and condition) and life-history (age) traits; (ii) variation in the tradeoff between the number and the size of eggs; (iii) seasonal effects and within-season differences in the timing of deposition. At the population level, we found no evidence for a tradeoff between the number and the size of eggs, because they both correlated positively with females’ body size. Conversely, neither age nor post-spawning body condition showed any effect on female reproductive investment. Independent of body size, we found no evidence for variation in reproductive effort among different breeding seasons, but strong evidence for a decrease of clutch size and an increase of egg size with the advancing of a breeding season. To test for the functional significance of the observed temporal variation in allocation strategy, we carried out a rearing experiment in semi-natural conditions on a random sample of ten clutches. The experiment showed a negative effect of clutch size and a positive effect of egg size on both tadpole growth and developmental rates, suggesting that reproductive investment, although constrained by body size, can be adjusted by females to the time of deposition to increase the chances of offspring survival.     

Female reproductive characteristics of the Balkan wall lizard (<Emphasis Type="Italic">Podarcis taurica</Emphasis>) in the northwestern periphery of its range

We present data on the female reproductive traits of the Balkan wall lizard in the Deliblato Sand, a large continental sandland in the Pannonian area in the northwestern periphery of the species range. The clutch and egg characteristics of the population were investigated on the basis of clutches laid in laboratory conditions by gravid females captured in one locality. Balkan wall lizards produced at least two clutches in a breeding season. Individual females laid clutches of commonly two (range 1–4) eggs. The female body size had no effect on clutch and egg size. There was no trade-off between egg size and clutch size.     

Not putting all their eggs in one basket: bet‐hedging despite extraordinary annual reproductive output of desert tortoises

Bet‐hedging theory makes the counter‐intuitive prediction that, if juvenile survival is low and unpredictable, organisms should consistently reduce short‐term reproductive output to minimize the risk of reproductive failure in the long‐term. We investigated the long‐term reproductive output of an Agassiz's desert tortoise (Gopherus agassizii) population and conformance to a bet‐hedging strategy of reproduction in an unpredictable but comparatively productive environment. Most females reproduced every year, even during periods of low precipitation and poor germination of food plants, and the mean percentage of reproducing females did not differ significantly on an annual basis. Although mean annual egg production (clutch size × clutch frequency) differed significantly among years, mean clutch size and mean clutch frequency remained relatively constant. During an El Niño year, mean annual egg production and mean annual clutch frequency were the highest ever reported for this species. Annual egg production was positively influenced by maternal body size but clutch size and clutch frequency were not. Our long‐term results confirm earlier conclusions based on short‐term research that desert tortoises have a bet‐hedging strategy of producing small clutches almost every year. The risk of long‐term reproductive failure is minimized in unpredictable environments, both through time by annually producing multiple small clutches over a long reproductive lifespan, even in years of low resource availability, and through space by depositing multiple annual clutches in different locations. The extraordinary annual reproductive output of this population appears to be the result of a typically high but unpredictable biomass of annual food plants at the site relative to tortoise habitat in dryer regions. Under the comparatively productive but unpredictable conditions, tortoises conform to predictions of a bet‐hedging strategy of reproduction with relatively small but consistent clutch sizes. Published 2015. This article is a U.S. Government work and is in the public domain in the USA, Biological Journal of the Linnean Society, 2015, 115 , 399–410.     

Insular shifts and trade-offs in life-history traits in pond frogs in the Zhoushan Archipelago, China

Island and mainland populations of animal species often differ strikingly in life-history traits such as clutch size, egg size, total reproductive effort and body size. However, despite widespread recognition of insular shifts in these life-history traits in birds, mammals and reptiles, there have been no reports of such life-history shifts in amphibians. Furthermore, most studies have focused on one specific life-history trait without explicit consideration of coordinated evolution among these intimately linked life-history traits, and thus the relationships among these traits are poorly studied. Here we provide the first evidence of insular shifts and trade-offs in a coordinated suite of life-history traits for an amphibian species, the pond frog Rana nigromaculata . Life-history data were collected from eight islands in the Zhoushan Archipelago and neighboring mainland China. We found consistent, significant shifts in all life-history traits between mainland and island populations. Island populations had smaller clutch sizes, larger egg sizes, larger female body size and invested less in total reproductive effort than mainland populations. Significant negative relationships were found between egg size and clutch size and between egg size and total reproductive effort among frog populations after controlling for the effects of body size. Therefore, decreased reproductive effort and clutch size, larger egg size and body size in pond frogs on islands were selected through trade-offs as an overall life-history strategy. Our findings contribute to the formation of a broad, repeatable ecological generality for insular shifts in life-history traits across a range of terrestrial vertebrate taxa.     

安徽滁州雌性丽斑麻蜥繁殖特征

在安徽滁州地区丽斑麻蜥(Eremias argus)年产两窝卵。窝卵数及窝卵重与雌体体长呈正相关,相对窝卵重与雌体体长无关,卵重与窝卵数无关。窝卵数、窝卵重及卵重在窝序间无明显的差异。卵长径与卵短径呈正相关,卵长径与窝卵数呈负相关,而卵短径与窝卵数无关。雌体主要通过增加窝卵数增加繁殖输出。     

Reproductive performance of a lacertid lizard at the core and the periphery of the species' range

The range boundaries of organisms are frequently interpreted in terms of a decline in the extent to which the life histories of outer populations are able to adapt to local environmental conditions. To test this hypothesis, we compared the reproductive characteristics of two Iberian populations of the lizard Psammodromus algirus (Linnaeus, 1758). One of them (Lerma) is close to the northern edge of the species' range, whereas the other one (El Pardo) occupies a typical core habitat 200 km further south. Gravid females were captured in the field and transported to the lab for egg laying. Second clutches were less frequent at Lerma (where clutch size and clutch mass were larger for first than for second clutches) than at El Pardo. The total mass of both clutches combined was similar at both sites. Thus, the higher frequency of second clutches at El Pardo appeared to balance the between-sites difference in energy allocation to the first clutch. Females from Lerma laid more but smaller eggs than those from El Pardo. When incubated at the same temperature, eggs from Lerma hatched sooner even when controlling for between-sites differences in mean egg size. These differences are interpreted in the light of the advantages of early hatching and high fecundity in the northern population, as opposed to large offspring size in the core population. We conclude that the life-history traits studied show enough variation, presumably of an adaptive nature, to cope with environmental challenges at the edge of the species' range.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 87–96.     

Cross‐generational costs of compensatory growth in nine‐spined sticklebacks

Compensatory growth (CG) is a form of phenotypic plasticity allowing individuals’ growth trajectories to rebound after a period of resource limitation, but little is known about the reproductive and cross‐generational costs of CG. We studied the potential costs of CG by exposing female nine‐spined sticklebacks Pungitius pungitius to 1) high (favourable), 2) low (stressful), and 3) recovery (initially stressful, subsequently favourable) feeding treatments, and quantified the effects of these treatments on female reproductive traits (clutch, egg and yolk size), and on the size of their offspring. The low feeding treatment reduced female size relative to the high and recovery feeding treatments, which produced equally large females. Hence, females from the recovery treatment demonstrated CG and full growth compensation. Feeding treatments had significant effects on clutch, yolk, egg and larval size, also when the effect of female size was controlled for. However, these effects came about mostly because females from the low feeding treatment produced small clutches with large eggs (containing little yolk) and larvae, whereas females from the recovery feeding treatment produced as large clutches, eggs (with similar amounts of yolk) and larvae as females from the high feeding treatment. Yet, structural equation modelling revealed that while a direct effect of female size on offspring size was positive in the low and high feeding treatments, it was negative in the recovery feeding treatment, independently of egg and clutch size. This indicates a cross‐generational tradeoff between female and offspring sizes in the recovery feeding treatment. Also the tradeoff between clutch and larval size was more pronounced in recovery than in low or high feeding treatments. Hence, apart from demonstrating that environmental influences experienced by females during their development have the potential to influence their size, fecundity and reproductive traits, the results also provide evidence for complex cross‐generational costs of recovery growth.