Phenotypic plasticity in reproductive traits induced by food availability in a lacertid lizard, Takydromus septentrionalis

Understanding the proximate determinants of phenotypic variations in life-history traits can provide powerful insights into a species' life-history strategies. I experimentally manipulated availability of food (high vs low) to examine plasticity in the reproductive traits of northern grass lizards, Takydromus septentrionalis (Lacertidae), from eastern China. Food availability significantly affected reproductive frequency and thereby seasonal reproductive output, but had little effect on reproductive output per clutch. Low-food females postponed reproduction and produced less clutches in the reproductive season than did high-food females. After producing their second clutches, low-food females were in lower body condition than the high-food counterparts. By the end of the experiment, however, all females exhibited similar body condition. Clutch size and clutch mass differed between the first and second clutches but not between the treatments. Egg size and phenotypic traits of hatchlings (body size, morphology and locomotor performance) in T. septentrionalis did not vary significantly from first to second clutches nor between the two treatments. These results support optimal egg size (offspring) theory. Female T. septentrionali s "decide" whether or not to reproduce largely based on current energy intake; lowered feeding rates thus delay oviposition and reduce reproductive frequency. In contrast, clutch size, egg size and relative clutch mass remain unchanged.     

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.     

Decline in the frequency and benefits of multiple brooding in great tits as a consequence of a changing environment

For multiple-brooded species, the number of reproductive events per year is a major determinant of an individual''s fitness. Where multiple brooding is facultative, its occurrence is likely to change with environmental conditions, and, as a consequence, the current rates of environmental change could have substantial impacts on breeding patterns. Here we examine temporal population-level trends in the proportion of female great tits (Parus major) producing two clutches per year (‘double brooding’) in four long-term study populations in The Netherlands, and show that the proportion of females that double brood has declined in all populations, with the strongest decline taking place in the last 30 years of the study. For one of the populations, for which we have data on caterpillar abundance, we show that the probability that a female produces a second clutch was related to the timing of her first clutch relative to the peak in caterpillar abundance, and that the probability of double brooding declined over the study period. We further show that the number of recruits from the second clutch decreased significantly over the period 1973–2004 in all populations. Our results indicate that adjustment to changing climatic conditions may involve shifts in life-history traits other than simply the timing of breeding.     

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.     

One clutch or two clutches? Fitness correlates of coexisting alternative female life-histories in the European earwig

Whether to reproduce once or multiple times (semelparity vs. iteroparity) is a major life-history decision that organisms have to take. Mode of parity is usually considered a species characteristic. However, recent models suggested that population properties or condition-dependent fitness payoffs could help to maintain both life-history tactics within populations. In arthropods, semelparity was also hypothesised to be a critical pre-adaptation for the evolution of maternal care, semelparous females being predicted to provide more care due to the absence of costs on future reproduction. The aim of this study was to characterize potential fitness payoffs and levels of maternal care in semel- and itero-parous females of the European earwig Forficula auricularia. Based on 15 traits measured in 494 females and their nymphs, our results revealed that iteroparous females laid their first clutch earlier, had more eggs in their first clutch, gained more weight during the 2 weeks following hatching of the first clutch, but produced eggs that developed more slowly than semelparous females. Among iteroparous females, the sizes of first and second clutches were significantly and positively correlated, indicating no investment trade-off between reproductive events. Iteroparous females also provided more food than semelparous ones, a result contrasting with predictions that iteroparity is incompatible with the evolution of maternal care. Finally, a controlled breeding experiment reported full mating compatibility among offspring from females of the two modes of parity, confirming that both types of females belong to one single species. Overall, these results indicate that alternative modes of parity represent coexisting life-history tactics that are likely to be condition-dependent and associated with offspring development and specific levels of maternal care in earwigs.     

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.     

蓝尾石龙子杭州和宁德种群繁殖生活史特征的差异

测定处于不同纬度的浙江杭州和福建宁德的蓝尾石龙子(Eumeceselegans)种群的个体大小和繁殖特征。宁德种群的产卵时间为5月27日—6月22日,早于高纬度杭州种群(6月4日—7月12日)。宁德种群最小繁殖雌体及性成熟个体大小均显著小于杭州种群。宁德和杭州两种群的相对窝卵重无显著差异;当统计去除母体体长的影响之后,两地种群的窝卵数和窝卵重也无显著差异,但杭州种群的卵重量显著大于宁德种群。蓝尾石龙子窝卵数和卵重量呈负相关,窝卵数和卵大小的权衡存在种群间差异。特定窝卵数条件下,杭州种群的卵重量显著大于宁德种群。由此可见,蓝尾石龙子种群间的繁殖生活史特征存在显著差异,而且与母体大小的差异密切相关。推测不同纬度地区的蓝尾石龙子种群的繁殖策略存在差异。     

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.     

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.     

蜡皮蜥的两性异形和繁殖输出

为研究蜡皮蜥(Leiolepis reevesii)两性异形和繁殖输出,于2002、2003年4月下旬从海南乐东一种群捕获423头蜡皮蜥。经检测得到繁殖雌体的最小体长为89．0mm,据此判定≥89．0mm的个体为性成熟。研究结果表明：①蜡皮蜥具有两性异形,雄性大于雌性且具有较大的头部。成体雄性头长和头宽随体长的增长速率大于雌性,幼体头长和头宽随体长的增长速率无显著的两性差异。以性别和年龄(成、幼体)为因子的双因子ANOVA比较两性头长和头宽与体长的回归剩余值发现,雄性头部大于雌性,幼体头部相对大于成体。②饲养于实验室的母体中有42头于2002、2003年5月22日～7月16日产出正常卵,这些繁殖雌体具有年产多窝卵的潜力。窝卵数和卵重的变异系数分别为0．18和0．13,前者变异度大于后者。窝卵数、窝卵重和卵重均与母体体长无关。卵重与相对生育力之间无显著的负相关性,表明蜡皮蜥缺乏卵数量与卵大小之间的权衡。相对窝卵重与母体体长呈显著的负相关,表明较小的母体具有相对较大的繁殖输出。因雌体繁殖会滞缓其生长,小母体具有相对较大的繁殖输出,至少部分地解释了雌性蜡皮蜥的成体为什么个体较小。     

Interpopulation variation in life-history traits of Poeciliopsis prolifica: implications for the study of placental evolution

Placental reproduction is widespread across vertebrate taxa, but little is known about its life-history correlates and putative adaptive value. We studied variation in life-history traits in two populations of the placental poeciliid fish Poeciliopsis prolifica to determine whether differences in post-fertilization maternal provisioning to embryos have a genetic basis and how food availability affects reproduction. Life histories were characterized for wild-caught females and for second-generation lab-born females raised under two levels of food availability. We found that the two populations did not differ significantly in the wild for any life-history traits except for the lipid dry weight in females and in embryos at an advanced stage of development. When environmental effects were experimentally controlled, however, populations exhibited significant differences in several traits, including the degree of maternal provisioning to embryos. Food availability significantly affected female size at first parturition, brood size and offspring dry weight at birth. Altogether, these results demonstrate that population differences in maternal provisioning and other life-history traits have a genetic basis and show a plastic response to food availability. We infer that phenotypic plasticity may mask population differences in the field. In addition, when comparing life-history patterns in these two populations with known patterns in placental and non-placental poeciliids, our results support the hypotheses that placentation is an adaptive reproductive strategy under high-resource conditions but that it may represent a cost under low-food conditions. Finally, our results highlight that age at maturity and reproductive allotment may be key life-history traits accompanying placental evolution.     

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.     

Variation of clutch size and trophic egg proportion in a ladybird with and without male-killing bacterial infection

Maternally inherited bacterial endosymbionts can kill male embryos of their arthropod hosts to enhance the transmission efficiency of the endosymbionts. The resources from killed male eggs can be reallocated to infected female hatchlings as additional maternal investment. As a result, the number of offspring per patch and the maternal investment per offspring are expected to differ from the original optimal values for the host mother. Thus, in response to infection, these trait values should be adjusted to maximize the lifetime reproductive success of host females and the fitness of inherited endosymbionts as well. Here, we examined clutch size, egg size, and the proportion of trophic eggs (i.e., production of unhatched eggs, a maternal phenotype) per clutch of host mothers infected with male-killing bacteria. First, we developed a mathematical model to predict the optimal clutch size and trophic egg proportion in uninfected and infected females. Next, we experimentally compared these life-history traits in a ladybird, Harmonia yedoensis, between females infected or uninfected with male-killing Spiroplasma bacteria. Consistent with our predictions, clutch size was larger, egg size was smaller, and trophic egg proportion was lower in infected H. yedoensis females, compared with uninfected females. To our knowledge, this is the first empirical demonstration of variation in these life-history traits depending on infection with bacterial endosymbionts.     

Female coloration indicates female reproductive capacity in blue tits

It is poorly understood whether female morphological and behavioural traits can be used as 'signals'. In particular, experimental tests of the hypothesis that female ornaments reflect quality are scarce. Here, we experimentally examine whether female plumage coloration might signal maternal quality in the blue tit, Cyanistes caeruleus by forcing half of the females breeding in our population to produce a replacement clutch. Using statistical models that controlled for the effects of male coloration, and the effects of age and condition of both parents, we found that carotenoid-based female coloration was positively linked to key proxies of bird lifetime reproductive success: clutch size, fledgling success and recruitment. Importantly, the relationships between maternal yellow carotenoid coloration and both clutch size and recruitment were stronger in the experimental group than in the control group, indicating that breeding females with higher values of yellow coloration were better able to handle the cost of producing a second clutch. Finally, UV-blue female coloration was positively linked to female survival and marginally linked to laying date. Taken together, these results show for the first time in a natural population that female coloration can indicate individual and maternal quality under natural and adverse reproductive conditions. They highlight the potential for the evolution of female ornamental traits through sexual selection.     

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.     

Clutch frequency affects the offspring size-number trade-off in lizards

Background

Studies of lizards have shown that offspring size cannot be altered by manipulating clutch size in species with a high clutch frequency. This raises a question of whether clutch frequency has a key role in influencing the offspring size-number trade-off in lizards.

Methodology/Principal Findings

To test the hypothesis that females reproducing more frequently are less likely to tradeoff offspring size against offspring number, we applied the follicle ablation technique to female Eremias argus (Lacertidae) from Handan (HD) and Gonghe (GH), the two populations that differ in clutch frequency. Follicle ablation resulted in enlargement of egg size in GH females, but not in HD females. GH females switched from producing a larger number of smaller eggs in the first clutch to a smaller number of larger eggs in the second clutch; HD females showed a similar pattern of seasonal shifts in egg size, but kept clutch size constant between the first two clutches. Thus, the egg size-number trade-off was evident in GH females, but not in HD females.

Conclusions/Significance

As HD females (mean  = 3.1 clutches per year) reproduce more frequently than do GH females (mean  = 1.6 clutches per year), our data therefore validate the hypothesis tested. Our data also provide an inference that maximization of maternal fitness could be achieved in females by diverting a large enough, rather than a higher-than-usual, fraction of the available energy to individual offspring in a given reproductive episode.     

Geographic variation in reproductive traits and trade-offs between size and number of eggs of the Chinese cobra (Naja atra)

We collected gravid Chinese cobras (Naja atra) from one island (Dinghai) and three mainland (Yiwu, Lishui and Quanzhou) populations in south‐eastern China to study geographical variation in female reproductive traits and the trade‐off between the size and number of eggs. We then conducted an common experiment on cobras from two of the four populations to further identify factors contributing to the observed trade‐offs. The mean size (snout–vent length) of the smallest five reproductive females increased with increasing latitude. Oviposition occurred between late June and early August, with females from the warmer localities laying eggs earlier than those from the colder localities. Maternal size was a major determinant of the reproductive investment in all populations, with larger females producing not only more but also larger eggs. Clutch size was more variable than egg size within and among populations. The observed geographical variation in clutch size, egg size, clutch mass and post‐oviposition body condition was not a simple consequence of variation in maternal size among populations, because interpopulation differences in these traits were still evident when the influence of maternal size was removed. The upper limit to reproductive investment was more likely to be set by the space availability in the island population, but by the resource availability in the three mainland populations. Trade‐offs between size and number of eggs were detected in all populations, with females that had larger clutches for their size having smaller eggs. Egg size at any given level of relative fecundity differed among populations, primarily because of interpopulation differences in the resource availability rather than the space availability. Except for the timing date of oviposition and the mean size of the smallest five reproductive females, all other examined traits did not vary in a geographically continuous trend. The common garden experiment, which standardized environmental factors, synchronized the timing date of oviposition, but it did not modify the conclusion drawn from the gravid females collected from the field. The observed geographical variation in the female reproductive traits could be attributed to the consequence of the effects of either proximate or ultimate factors. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85 , 27–40.     

Phenotypic selection and function of reproductive behavior in the subsocial bug Elasmucha putoni (Heteroptera: Acanthosomatidae)

To investigate the function of maternal care and determinantsof reproductive success in the subsocial bug Elasmucha putoni (Heteroptera: Acanthosomatidae), I used two different approaches,the measurement of phenotypic selection and female-removalexperiments under conditions differing in biotic-environmentalpressure. For two field populations, unattended eggs and youngernymphs consistently suffered severe predation pressure andattendance by parent females greatly enhanced their survival.In contrast, under enemy-excluded conditions, offspring performance was not reduced in broods without parent females, indicatingthat maternal care functions as a physical defense againstpredators. However, the determinant of female reproductivesuccess in E. putoni in the field was not the care behavioralone. Selection gradient analysis showed that early seasonoviposition and larger clutch size, as well as a longer durationof care by a female, was favored during the breeding episode.This study is the first to evaluate phenotypic selection onparental care and other reproductive traits in arthropods.     

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.     

Multiple Mating Increases Fecundity, Fertility and Relative Clutch Mass in the Female Leopard Gecko (Eublepharis macularius)

Females across many taxa may mate with several males or mate more than once with the same male within one reproductive event. Although many researchers have discussed the effects of multiple mating on reproductive success of females, few studies have attempted to disentangle whether the reproductive success of females differs with respect to whether females mate with multiple males or mate more than once with one male. In this study, we hypothesized that female leopard geckos (Eublepharis macularius) increase aspects of their reproductive success, such as fecundity, fertility and relative clutch mass, by mating more than once within one reproductive event, either by mating repeatedly with the same male or multiply mating with different males. We controlled for the potentially confounding variables of mating frequency and mate number by allowing females to mate once with one male, twice with the same male, or twice with two different males. We found that females that mated with more than one male laid more clutches, exhibited increased egg fertility and invested more in clutches relative to females that mated only once with one male, whereas females that mated twice to the same male were intermediate for these variables. Thus, reproductive success is higher among female leopard geckos that mated with more than one male compared to female leopard geckos that mated only once.