Longterm effects of incubation temperatures on the morphology and locomotor performance of hatchling lizards (Bassiana duperreyi, Scincidae)

The phenotypes of hatchling reptiles are known to be affected by the thermal environments they experience during incubation, but the evolutionary and ecological significance of this phenotypic plasticity remains unclear. Crucial issues include: (i) the magnitude of effects elicited by thermal regimes in natural nests (as opposed to constant-temperature incubation); (ii) the persistence of these effects during ontogeny; and (iii) the consistency of these effects across different test conditions (does the thermal regime during embryogenesis simply shift the hatchling's thermal optimum for performance, or actually modify overall performance ability regardless of temperature?). We examined these questions by incubating eggs of scincid lizards (Bassiana duperreyi) from montane southeastern Australia, under two fluctuating-temperature regimes that simulated ‘cold’ and ‘hot’ natural nests. These thermal regimes substantially modified hatchling morphology (mass, body length, tail length, and the relationship between these variables), locomotor performance (running speeds over distances of 25 cm and lm), anti-predator ‘tactics’ and survival rates. The differences in locomotor performance persisted throughout the 20 weeks of our experiment. Lizards that emerged after ‘hot’ incubation were faster runners than their ‘cold’-incubated siblings under all thermal conditions that we tested. Thus, incubation temperatures modified overall locomotor ability, with only a minor effect on the set-point for optimum performance. The magnitude, persistence and consistency of these incubation-induced phenotypic modifications suggest that they may play an important role in evolutionary and ecological processes within lizard populations.     

Matching field and laboratory environments: effects of neglecting daily temperature variation on insect reaction norms

The tropical butterfly, Bicyclus anynana, exhibits seasonal polyphenism. The wet season form has large eyespots and a pale band while these characters are much less conspicuous or absent in the dry season form. This plasticity is induced in the laboratory by use of a standard series of constant temperatures in the larval stage yielding a continuous norm of reaction. Butterflies in this study were reared from hatchling larvae in seven regimes which differed with respect to thermoperiod or photoperiod. The effect of rearing treatment on the phenotypic plasticity of the adult wing pattern, on life history traits and on larval feeding rhythms was investigated. Photoperiod had little effect except that constant light produced a higher mortality and tended to produce a longer development time. Thermoperiod had a major effect on the life history traits in comparison to a constant temperature regime with the same daily mean: development time was shorter with higher growth rates. The faster development was associated with a substantial shift in the wing pattern towards the wet season form. Larvae feed mostly at night both under constant and thermoperiod (cool nights) conditions. The results are discussed with respect to the necessity of matching field and laboratory environments in studies of norms of reaction or of life history traits where the adaptive significance of the variation is important. Fluctuating conditions in nature, especially with respect to thermoperiod, must be taken into account.     

Eggs in autumn: responses to declining incubation temperatures by the eggs of montane lizards

Facultative hatching in response to environmental cues may increase the viability of offspring, if the cue that stimulates hatching also predicts the negative consequences of delayed emergence. Declining incubation temperatures might provide such a cue for montane lizards, because eggs that fail to hatch before winter will perish in the nest. I tested this idea by incubating eggs of an alpine scincid lizard ( Bassiana duperreyi ) in the laboratory. For the first half of the incubation period the eggs were kept at nest temperatures typical of those experienced in summer in the field (daily cycle of 18 ± 7.5°C). I then transferred eggs at weekly intervals into cooler regimes (either 15 ± 7.5°C; or with daytime temperatures unchanged but dropping to 0°C overnight). Contrary to prediction, the eggs did not hatch early. However, transfer to lower temperatures caused only a relatively short delay in hatching, because of a virtual temperature-independence of developmental rates late (but not early) in incubation. Decreasing incubation temperatures also modified hatchling running speeds and post-hatching growth rates, even if the thermal decrease occurred only shortly before the usual time of hatching. These processes plausibly affect hatchling fitness in cold-climate reptiles, and might be adaptations to montane habitats. Alternatively, they may prove to be widespread in other (warmer-climate) reptile taxa, in which case no adaptive hypothesis need be proposed. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 76 , 71–77.     

Geographic variation in lizard phenotypes: importance of the incubation environment

Geographic variation in phenotypes can result from proximate environmental effects as well as from underlying genetic factors. Reciprocal transplant experiments, in which organisms are moved from one area to another, offer a powerful technique to partition the effects of these two factors. However, many studies that have utilized this technique have focused on the post-hatching organism only and ignored potential effects of environmental influences acting during embryonic development. We examined the phenotypic responses of hatchling scincid lizards ( Lampropholis guichenoti ) incubated in the laboratory under thermal regimes characteristic of natural nests in two study areas in southeastern Australia. Although the sites were less than 120 km apart, lizards from these two areas differed in thermal regimes of natural nests, and in hatchling phenotypes (morphology, locomotor performance). We incubated eggs from each area under the thermal regimes typical of both sites. Some of the traits we measured (e.g. hatchling mass and snout-vent length) showed little or no phenotypic plasticity in response to differences in incubation conditions, whereas other traits (e.g. incubation period, tail length, inter-limb length, body shape, locomotor performance) were strongly influenced by the thermal regime experienced by the embryo. Thus, a significant proportion of the geographic variation in morphology and locomotor performance of hatchling lizards may be directly induced by differences in nest temperatures rather than by genetic divergence. We suggest that future studies using the reciprocal transplant design should consider environmental influences on all stages of the life-history, including embryonic development as well as post-hatching life.     

Emergence of sexual size dimorphism and stage‐specific effects of elevated temperature on growth rate and development rate in Harmonia axyridis

Temperature is considered to be the most important environmental factor influencing the performance of ectotherms because it determines the rate of most biochemical reactions and thus the efficiency of metabolism and its function. Unfortunately, most studies investigate the effects of temperature on individuals exposed to a particular temperature regime during their whole pre‐imaginal development and detailed information on variation of the temperature effects during ontogeny is rare. In the present study, the effects of the timing of exposure to a transient period of elevated temperature during ontogeny on development rate and growth rate are investigated for the ladybird Harmonia axyridis Pallas. Control beetles are reared at a constant temperature of 20 °C, whereas treated beetles are reared at 20 °C but are exposed to 33 °C for 48 h either during the early‐larval stage, third‐larval instar, fourth‐larval instar or the pupal stage. The rate of development and the growth rate are both accelerated because the timing of exposure to elevated temperature occurred later in pre‐imaginal development (i.e. development rate and growth rate are highest in individuals exposed to elevated temperature during the pupal stage). An exception to this pattern is the lowering of development rate in individuals exposed to elevated temperature during the fourth‐larval instar. Female H. axyridis have a significantly higher development rate and growth rate than males. However, the relative difference in growth rate between the sexes is much higher than the difference in development rate between sexes, resulting in a female‐biased size (mass) dimorphism in adult beetles.     

Sexual size dimorphism decreases with temperature in a blowfly,Chrysomya megacephala (Fabricius) (Diptera: Calliphoridae)

1. There is wide intra‐specific variation in sexual size dimorphism (SSD). Much of this variation is probably as a result of sexual differences in the selective pressure on body size. However, environmental variables could affect males and females differently, causing variation in SSD. 2. We examined the effects of two temperatures (20 and 30 °C) on SSD in six populations of the blowfly, Chrysomya megacephala. 3. We found that body size increased with temperature in all the populations studied, and the sexes differed in phenotypic plasticity of body size in response to rearing temperature. This created substantial temperature‐induced variation in SSD (i.e. sex × temperature interaction). Males were often smaller than females, but the degree of dimorphism was smaller at the higher temperature (30 °C) and larger at the lower temperature (20 °C). This change in SSD was not because of a gender difference in the effect of temperature on development time. Further studies should address whether this variation can be produced by adaptive canalisation of one sex against variation in temperature, or whether it may be a consequence of non‐adaptive developmental differences between the sexes. 4. Although most studies assume that the magnitude of SSD is fixed within a species, the present study demonstrates that rearing temperature can generate considerable intra‐specific variation in the degree of SSD.     

Geographic variation in hatchling size in an oviparous skink: effects of maternal investment and incubation thermal environment

Geographic variation in offspring size can be viewed as an adaptive response to local environmental conditions, but the causes of such variation remain unclear. Here, we compared the size and composition of eggs laid by female Chinese skinks (Plestiodon chinensis) from six geographically distinct populations in southeastern China to evaluate geographic variation in hatchling size. We also incubated eggs from these six populations at three constant temperatures (24, 28 and 32 °C) to evaluate the combined effects of incubation temperature and population source on hatchling size. Egg mass and composition varied among populations, and interpopulation differences in yolk dry mass and energy content were still evident after accounting for egg mass. Population mean egg mass and thus hatchling mass were greater in the colder localities. Females from three northern populations increased offspring size by laying larger eggs relative to their own size. Females from an inland population in Rongjiang could increase offspring size by investing relatively more dry materials and thus more energy into individual eggs without enlarging the size of their eggs. The degree of embryonic development at oviposition was almost the same across the six populations, so was the rate of embryonic development and thus incubation length at any given temperature. Both incubation temperature and population source affected hatchling traits examined, but the relative importance of these two factors varied between traits. Our data show that in P. chinensis hatchling traits reflecting overall body size (body mass, snout‐vent length and tail length) are more profoundly affected by population source. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 283–296.     

Genetic variation and plasticity of thorax length and wing length in Drosophila aldrichi and D. buzzatii

Reaction norms across three temperatures of development were measured for thorax length, wing length and wing length/thorax length ratio for ten isofemale lines from each of two populations of Drosophila aldrichi and D. buzzatii. Means for thorax and wing length in both species were larger at 24 °C than at either 18 °C or 31 °C, with the reduction in size at 18 °C most likely due to a nutritional constraint. Although females were larger than males, the sexes were not different for wing length/thorax length ratio. The plasticity of the traits differed between species and between populations of each species, with genetic variation in plasticity similar for the two species from one locality, but much higher for D. aldrichi from the other. Estimates of heritabilities for D. aldrichi generally were higher at 18 °C and 24 °C than at 31 °C, but for D. buzzatii they were highest at 31 °C, although heritabilities were not significantly different between species at any temperature. Additive genetic variances for D. aldrichi showed trends similar to that for heritability, being highest at 18 °C and decreasing as temperature increased. For D. buzzatii, however, additive genetic variances were lowest at 24 °C. These results are suggestive that genetic variation for body size characters is increased in more stressful environments. Thorax and wing lengths showed significant genetic correlations that were not different between the species, but the genetic correlations between each of these traits and their ratio were significantly different. For D. aldrichi, genetic variation in the wing length/thorax length ratio was due primarily to variation in thorax length, while for D. buzzatii, it was due primarily to variation in wing length. The wing length/thorax length ratio, which is the inverse of wing loading, decreased linearly as temperature increased, and it is suggested that this ratio may be of greater adaptive significance than either of its components.     

Thermally induced plasticity of body shape in adult zebrafish Danio rerio (Hamilton, 1822)

We examined the effect of temperature during the early development on the phenotypic plasticity of Danio rerio. The effect of temperature was examined during two different early developmental periods of 280°d (the product of days × temperature) each, 28‐308°d or 280‐560°d, by subjecting the experimental populations to three different water temperatures (22°C, 28°C, and 32°C). Before and after the end of the 280°d period of the different thermal exposure, all populations were cultured in standard temperature (28°C). Five to 10 months after exposure to the different thermal regimes, the body shape of the adults was analyzed by geometric morphometrics. In both ontogenetic windows and experimental repetitions, the results showed that developmental temperature and sex significantly affected the body shape of adult zebrafish. Thermally induced shape variation discriminated the fish that developed at 22°C from those developed at 28°C–32°C. In the early developmental period (DP1, 28–308°d postfertilization), dorsal, anal, and caudal fin structures differed between the animals that developed at 22°C and 28°C–32°C. In the later developmental period (DP2, 280–560°d postfertilization), caudal, anal, pectoral, and pelvic fins, as well as the gill cover and lower jaw, were affected when animals developed at different temperatures. These results show that thermal history during a short period of embryonic and larval life affects the body form of adult zebrafish with potentially functional consequences. Based on previous data on the effects of temperature on fish development, we suggest thermally induced muscle and bone remodelling as possible mechanism underlying the observed plasticity. J. Morphol., 2010. © 2010 Wiley‐Liss, Inc.     

How a thermal dichotomy in nesting environments influences offspring of the world's most northerly oviparous snake,Natrix natrix (Colubridae)

Temperature has a major influence on the rate of embryonic development in ectothermic organisms. While incubation experiments unambiguously show that constant high temperature accelerates development and shortens embryonic life, studies on the effect of fluctuating temperatures have generated contradictory results. Grass snakes (Natrix natrix) occur at latitudes and altitudes that are unusually cool for an oviparous reptile. In these cool climates females typically lay their eggs in heat‐generating anthropogenic microhabitats that provide either a highly fluctuating (compost piles) or a relatively constant (manure heaps) thermal nesting environment. A laboratory experiment with fluctuating and constant incubation temperatures mimicking those recorded in such nests in the field showed that this nest‐site dichotomy influences the development of the embryos, and the morphology and locomotor performance of the hatchlings. The incubation period increased at fluctuating temperatures and the fact that the rate of embryonic development showed a decelerating pattern with temperature suggests that periods of low temperature had a relatively larger influence on average development than periods of high temperature. Our study demonstrates how a dichotomy in the nesting environments available to female grass snakes in cool climates can affect variation in the duration of the incubation period and offspring phenotypes in ways that may have consequences for fitness. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ??, ??–??.     

水热环境对白条草蜥孵化卵和孵出幼体表型特征的影响

用4×2(温度×湿度)八种水热环境孵化安徽滁州琅琊山白条草蜥(Takydromus wolteri)卵,观测孵化卵重量变化、胚胎利用卵内物质和能量以及孵出幼体的特征。卵从孵化环境中吸水导致重量增加,卵重量的增加与入孵卵重量、孵化温度和基质湿度有关。两种孵化基质湿度对孵化期、孵化成功率、孵出幼体性比和大小都无显著影响。孵化期随恒定孵化温度的升高而缩短,27℃、30℃和33℃孵化期分别为32.5、24.9和23.0d,波动温度孵化期为31.1d。33℃孵化成功率最低(42.8%)。温度对孵化成功率和孵出幼体的性别无显著影响,但显著影响胚胎对卵内物质的动用、幼体的大小和重量。33℃不适宜孵化白条草蜥卵,该温度下孵出的幼体躯干小,剩余卵黄多,运动能力差。27℃和波动温度中孵出幼体躯干发育良好,各项被测定的特征指标极其相似。     

不同水温条件下中华蟾蜍蝌蚪的表型可塑性研究

对中华蟾蜍Bufo gargarizans蝌蚪在不同水温下生长以及变态情况进行了观察,测量了不同发育时期的全长、尾长、体宽,记录了不同温度条件下各时期出现的起始时间和持续时间;比较了不同温度条件下的发育状态,发现高温可以明显加速生长,比对照组提前17天变态.方差分析得出高温下变态前的体长、尾长、体宽、尾高、前肢长都与对照组有明显差异（P＜0.01）,说明高温虽然加速了生长,但也使得变态能量积累不够,体形偏小;21℃时,全长、尾长与对照组差异不显著,其余变量差异显著,说明这个温度下,蝌蚪发育时间充足,积累能量多,趋向于形成较大的个体.这种在水温变化时所呈现出来的表型可塑性有利于适应异质性的环境,急速发育导致的提前变态可以使其避开干旱的危害.但是这种表型可塑性能力也有其局限,推测小个体的成体可能会在生长繁殖中付出代价.     

Rule of age and size at maturity: individual variation in the maturation history of resident white-spotted charr

Individual growth and maturation histories, age, and size at maturity of resident white-spotted charr Salvelinus leucomaenis were examined in a tag-recapture study in a natural river over 3 years. Slow-growing fish reached sexual maturity not only at an older age, but also at a smaller size than fast-growing fish, although females had a larger threshold size at maturity than males at each age. It is suggested that these patterns result from adaptive phenotypic plasticity that depends on individual growth conditions.     

Seasonal phenotypic plasticity of wing melanisation in the cabbage white butterfly, Pieris rapae L. (Lepidoptera: Pieridae)

Abstract.  1. Effective thermoregulation is crucial for the fitness of small flying insects. Phenotypic plasticity of the ventral hindwing of pierid butterflies is widely recognised as adaptive for effective thermoregulation. Butterflies eclosing in cooler environments have more heavily melanised wings that absorb solar radiation, thus allowing flight under these cool conditions.
2. Many pierids also exhibit phenotypic plasticity of dorsal forewing melanisation but in this case, cooler environments reduce melanisation. It has been hypothesised that this plasticity is also adaptive because it increases solar reflection from the wing surfaces onto the body in certain basking postures.
3. The degree of seasonal variation in ventral hindwing and dorsal forewing melanisation of wild-caught Pieris rapae was quantified to determine if it shows patterns of plasticity similar to that documented for other Pieris species.
4. Male wing melanisation on both wing surfaces shows the characteristic seasonal, adaptive plasticity. However, only some dorsal forewing pattern elements of females conformed to the predictions of the hypothesis of adaptive dorsal forewing melanisation. Sexual dimorphism of wing pattern plasticity may result from, and/or affect, sexual dimorphism of behaviour and physiology of these butterflies.     

Phenotypic variation in colour pattern and seasonal plasticity in Eristalis hoverflies (Diptera: Syrphidae)

Abstract.

• 1 An examination of phenotypic variation in colour pattern was carried out on four Eristalis hoverfly species using museum material.
• 2 The amount of phenotypic variation varied substantially among the species with E.arbustorum being the most variable. The other species showed a wide colour pattern range but less variation within that range (E.abusivus and E.nemorum), or a narrow range of colour variation (E.horticola).
• 3 Sexual colour dimorphism was apparent in all four species, but most pronounced in E.abusivus and E.nemorum.
• 4 There were good phenotype-season relationships shown by both sexes in all species, except for female E.abusivus and E.nemorum, with paler insects being more abundant during the warmer summer months.
• 5 Female, but not male, E.arbustorum collected at inland sites were on average paler than those collected at coastal sites. This observation is considered with respect to temperature during the developmental stages.
• 6 The function of colour plasticity in hoverflies is discussed with reference to the need to maintain optimal thermal conditions for activity.

     

Plasticity and limitations of extended egg retention in oviparous Zootoca vivipara (Reptilia: Lacertidae)

The transition between oviparity and viviparity in reptiles is generally accepted to be a gradual process, the result of selection for increasingly prolonged egg retention within the oviduct. We examined egg retention plasticity in an oviparous strain of the lacertid lizard Zootoca vivipara, a species having both oviparous and viviparous populations. We forced a group of female Z. vivipara to retain their clutch in utero by keeping them in dry substrata, and assessed the effect on embryonic development and hatching success, along with offspring phenotype and locomotor performance. Forced egg retention for one additional week affected the developmental stage of embryos at oviposition, as well as hatchling robustness and locomotor performance. However, embryos from forced clutch retention treatment reached one stage unit more than control embryos at oviposition time. Embryos from control eggs were more developed than embryos from experimental eggs after approximately the same period of external incubation, showing that embryonic development is retarded during the period of extended egg retention, despite the high temperature inside the mother's body. Significant differences in external incubation time were only found in one of the two years of study. Hatching success was much lower in the experimental group with forced egg retention (21.1%) than in the control group (95.4%). Therefore, we conclude that there are limitations that hinder the advance of intrauterine embryonic development beyond the normal time of oviposition, and that extended egg retention does not represent clear advantages in this population of Z. vivipara. Nevertheless, the fact that some eggs are successful after forced egg retention could be advantageous for the females that are able to retain their clutch under unfavourable climatic conditions. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 75–82.     

Inter- and intra-sexual variation in immune defence in the cabbage white butterfly, Pieris rapae L. (Lepidoptera: Pieridae)

Abstract.  1. Immune defence imposes fitness costs as well as benefits, so organisms are expected to optimise, not maximise, their immune responses. This should result in variation in immune responses under varying environmental conditions.
2. Males and females are expected to exhibit different immune responses because life-history differences between the sexes affect optimal immune response. These life-history differences should usually result in a greater female, than male, immune defence. In this study, intra- and inter-sexual variation in one component of immune defence, the encapsulation response, in cabbage white butterflies ( Pieris rapae L.), was examined.
3. Encapsulation decreased with increasing age and in response to reduced diet quality.
4. Contrary to predictions, males generally had greater immune responses than females, although this pattern varied with age.
5. These patterns of inter- and intra-sexual variation in encapsulation may result from resource-based trade-offs with components of reproductive effort and/or because of sexual dimorphism in melanin-based wing patterns.     

Functional and ecological relevance of intraspecific variation in body size and shape in the lizard Podarcis melisellensis (Lacertidae)

Within populations, individual animals may vary considerably in morphology and ecology. The degree to which variation in morphology is related to ecological variation within a population remains largely unexplored. We investigated whether variation in body size and shape among sexes and age classes of the lizard Podarcis melisellensis translates in differential whole-animal performance (sprint speed, bite force), escape and prey attack behaviour in the field, microhabitat use and diet. Male and female adult lizards differed significantly in body size and head and limb proportions. These morphological differences were reflected in differences in bite strength, but not in sprint speed. Accordingly, field measurements of escape behaviour and prey attack speed did not differ between the sexes, but males ate larger, harder and faster prey than females. In addition to differences in body size, juveniles diverged from adults in relative limb and head dimensions. These shape differences may explain the relatively high sprint and bite capacities of juvenile lizards. Ontogenetic variation in morphology and performance is strongly reflected in the behaviour and ecology in the field, with juveniles differing from adults in aspects of their microhabitat use, escape behaviour and diet.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 251–264.