Seasonal plasticity in life history traits: growth and development in Polygonia c-album (Lepidoptera: Nymphalidae)

The potentially multivoltine comma butterfly, Polygonia c-album L., hibernates in the adult stage. The adult seasonal morph is demonstrated to be a good indicator of whether an individual has entered reproductive diapause or is developing directly to sexual maturation. This fact, and the assumption that a short development time is not equally important to all categories of individuals, was used to test predictions on variation in life-history traits among categories (morphs and sexes) and environments (temperature and photoperiod) at the level of individuals and to some extent families and populations (the univoltine Stockholm population and the partially bivoltine Oxford population). Individuals developing to adults in a short time were expected to be smaller and lighter as a result of a basic trade-off between the two traits. Development times varied in accordance with predictions, but in most cases this was due to plastic growth and development in both the larval and pupal stages rather than through variation in size or weight, i.e. size was a highly canalized trait. This suggests a relationship between plasticity and canalization and a strong potential for plasticity to shield life-history traits from selection. Individuals regulated development times also within developmental pathways, in response to photoperiods indicating the progression of the season. These and other results suggest that development times are not normally minimized in temperate butterflies unless this is enforced by direct development and protandry. There is thus scope for a high degree of adaptive plasticity in growth- and developmental rates which may devalue the basic trade-offs assumed by life-history theory and account for inconsistencies with its predictions.     

Distinguishing between anticipatory and responsive plasticity in a seasonally polyphenic butterfly

Seasonal generations of short-lived organisms often differ in their morphological, behavioural and life history traits, including body size. These differences may be either due to immediate effects of seasonally variable environment on organisms (responsive plasticity) or rely on presumably adaptive responses of organisms to cues signalizing forthcoming seasonal changes (anticipatory plasticity). When directly developing individuals of insects are larger than their overwintering conspecifics, the between-generation differences are typically ascribed to responsive plasticity in larval growth. We tested this hypothesis using the papilionid butterly Iphiclides podalirius as a model species. In laboratory experiments, we demonstrated that seasonal differences in food quality could not explain the observed size difference. Similarly, the size differences are not likely to be explained by the immediate effects of ambient temperature and photoperiod on larval growth. The qualitative pattern of natural size differences between the directly developing and diapausing butterflies could be reproduced in the laboratory as a response to photoperiod, indicating anticipatory character of the response. Directly developing and diapausing individuals followed an identical growth trajectory until the end of the last larval instar, with size differences appearing just a few days before pupation. Taken together, various lines of evidence suggest that between-generation size differences in I. podalirius are not caused by immediate effects of environmental factors on larval growth. Instead, these differences rather represent anticipatory plasticity and are thus likely to have an adaptive explanation. It remains currently unclear, whether the seasonal differences in adult size per se are adaptive, or if they constitute co-product of processes related to the diapause. Our study shows that it may be feasible to distinguish between different types of plasticity on the basis of empirical data even if fitness cannot be directly measured, and contributes to the emerging view about the predominantly adaptive nature of seasonal polyphenisms in insects.     

Artificial selection on the shape of reaction norms for eyespot size in the butterfly Bicyclus anynana: direct and correlated responses

The tropical butterfly Bicyclus anynana shows phenotypic plasticity in its ventral wing pattern as an adaptive response to wet‐dry seasonality. Wet season form individuals have large eyespots, whereas individuals of the dry season generation have small eyespots. In the laboratory these forms can be obtained by rearing larvae at high and low temperatures, respectively. To study the extent to which the shape of the nearly linear reaction norms for eyespot size can be changed we applied four generations of sib selection by rearing full‐sib families across three temperatures. In addition, we measured ecdysteroid titres shortly after pupation in the final generation. Although phenotypic variation in shape was present initially, the experiment yielded lines with reaction norms with similar shapes but different elevations. High, positive genetic correlation across temperatures can explain this lack of response. Differences in ecdysteroid titres did not readily relate to differences in eyespot size.     

Counterintuitive size patterns in bivoltine moths: late-season larvae grow larger despite lower food quality

Within a season, successive generations of short-lived organisms experience different combinations of environmental parameters, such as temperature, food quality and mortality risk. Adult body size of e.g. insects is therefore expected to vary both as a consequence of proximate environmental effects as well as adaptive responses to seasonal cues. In this study, we examined intraspecific differences in body size between successive generations in 12 temperate bivoltine moths (Lepidoptera), with the ultimate goal to critically compare the role of proximate and adaptive mechanisms in determining seasonal size differences. In nearly all species, individuals developing late in the season (diapausing generation) attained a larger adult size than their conspecifics with the larval period early in the season (directly developing generation) despite the typically lower food quality in late summer. Rearing experiments conducted on one of the studied species, Selenia tetralunaria also largely exclude the possibility that the proximate effects of food quality and temperature are decisive in determining size differences between successive generations. Adaptive explanations appear likely instead: the larger body size in the diapausing generation may be adaptively associated with the lower bird predation pressure late in the season, and/or the likely advantage of large pupal size during overwintering.     

Phenotypic plasticity of starvation resistance in the butterfly <Emphasis Type="Italic">Bicyclus anynana</Emphasis>

Starvation resistance is an important trait related to survival in many species and often involves dramatic changes in physiology and homeostasis. The tropical African butterfly Bicyclus anynana lives in two seasonal environments and has evolved phenotypic plasticity. The contrasting demands of the favourable, wet season and the harsh, dry season have shaped a remarkable life history, which makes this species particularly interesting for investigating the relationship between starvation resistance, metabolism, and its environmental modulation. This study reports on two laboratory experiments to investigate the effects of pre-adult and adult temperatures that mimic the seasonal environments, on starvation resistance and resting metabolic rate (RMR) in adult B. anynana. In addition, we investigate starvation resistance in wet and dry seasonal form genotypes; artificial selection on eyespot size has yielded lines that only produce one or the other of the seasonal forms across all rearing environments. As expected, the results show a large effect of adult temperature. More relevant, we show here that both pre-adult temperature and genetic background also influence adult starvation resistance, showing that phenotypic plasticity in this species includes starvation resistance. The dry season form genotype has a higher starvation resistance when developed at dry season temperatures, indicating a genetic modulation of starvation resistance in relation to temperature. Paradoxically, dry season pre-adult temperatures reduce starvation resistance and raise RMR. The high overall association of RMR and starvation resistance in our experiments suggests that energy expenditure and survival are linked, but that they may counteract each other in their influence on fitness in the dry season. We hypothesize that metabolism is moderating a trade-off between pre-adult (larval) survival and adult survival in the dry season.     

Seasonal butterfly design: morphological plasticity among three developmental pathways relative to sex,flight and thermoregulation

The temperate‐zone butterfly Pararge aegeria can use three developmental pathways corresponding to different seasonal cohorts: (1) development with a pupal winter diapause resulting in early spring adults; (2) development with a larval winter diapause resulting in late‐spring adults and (3) direct development resulting in summer or second generation adults. In order to test adaptive predictions, we compared variation in flight‐ and thermoregulation‐related morphology among adult males and females from the three pathways using both field data (i.e. wild‐caught butterflies) and experimental breeding data (i.e. reared under different photoperiod regimes). Morphological patterns among the pathways were largely similar in the field and rearing data. Seasonal patterns differed between the sexes for most traits, including (relative) size measures and wing colour. Our results suggest sex‐related, adaptive seasonal plasticity for morphological traits related to flight behaviour in a multivoltine insect.     

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.     

Tropical dry and wet season polyphenism in the butterfly Melanitis leda (Satyrinae): Phenotypic plasticity and climatic correlates

Changes in wing pattern, colour, shape and size associated with seasonal polyphenism in Melanitis leda were quantified using a series of 155 butterflies collected by N. Manders on Mauritius in 1905. Butterflies of the wetter period were predominantly of the wet season form with large, well differentiated eyespots, short tails, smaller wings and a characteristic background colour. The dry season form occurred only in the drier period and has much smaller eyespots, longer tails, larger wings and a variable background. Many intermediates occurred, mainly in the drier period. These are associated with an absence of extreme seasonal change in Mauritius. The first principal component (PCI) describing the morphometric and colour data is closely related to the wing form (r = 0.80). Regression analyses using temperature and rainfall data for the 8 weeks before each capture showed that about 40% of variation in PCI could be accounted for by temperature in weeks 2–3 before capture. Many of the characters measured are redundant; a subset of seven morphometric characters yields a closely similar PCI. Analysis of is subset in an additional sample of 70 M. leda from Kenya showed that the seasonal polyphenism overrides a small degree of sexual dimorphism. The results are discussed with regard to seasonal changes in adult activity, resting backgrounds and visual predation. Wing phenotype characters are part of an array of coordinated morphological and life history traits which include ovarian dormancy and fat body development in dry season adults. A partial independence occurs in the proximal control of these traits as indicated, for example, by the larger wing and tail size, and smaller eyespots of the small number of the wet season form captured in the drier period in comparison to those of the wetter months.     

The evolutionary genetics of egg size plasticity in a butterfly

Abstract The evolution of phenotypic plasticity requires that it is adaptive, genetically determined, and exhibits sufficient genetic variation. For the tropical butterfly Bicyclus anynana there is evidence that temperature-mediated plasticity in egg size is an adaptation to predictable seasonal change. Here we set out to investigate heritability in egg size and genetic variation in the plastic response to temperature in this species, using a half-sib breeding design. Egg size of individual females was first measured at a high temperature 4 days after eclosion. Females were then transferred to a low temperature and egg size was measured after acclimation periods of 6 and 12 days respectively. Overall, additive genetic variance explained only 3-11% of the total phenotypic variance, whereas maternal effects were more pronounced. Genotype-environment interactions and cross-environmental correlations of less than unity suggest that there is potential for short-term evolutionary change. Our findings strengthen the support for the adaptive nature of temperature-mediated plasticity in egg size.     

Age‐ and sex‐related differences in the spatial ecology of a dichromatic tropical python (Morelia viridis)

Abstract: Despite outnumbering their temperate counterparts, tropical snake species have been poorly studied. Yet, the few tropical species that have been studied show a variety of behavioural traits beyond those described in temperate species. Here we reveal both age and sexual differences in the movements of tropical green pythons (Morelia viridis: Pythonidae). We radio‐tracked 27 individuals (17 females and 10 males) for up to 18 months, locating individuals during both the day and night. The home range size for adult females (mean ± SE of 6.21 ± 1.85 ha) was correlated with snout–vent length. Neither adult males nor juveniles had a stable home range. Adult females had stable home ranges that overlapped considerably with those of other females and yellow individuals. Multiple radio‐tracked adult males passed through the territory of radio‐tracked adult females during the study. Females of all sizes were more likely to change position each day than males. There were no differences between the sexes or size categories in the distances moved in most months, although the variation in movement distances was higher in the dry season than during the wet season. In the wet season (January–March) movement distances increased and these were size‐ and sex‐related. This increased activity may be associated with mate searching. Males of M. viridis may maximize their rate of encountering mature females by roaming rather than maintaining a home range. Juvenile green pythons moved distances equal to adult snakes in most months despite their comparatively small size.     

Abundance and Leaf Damage Caused by Gall‐Inducing Insects in a Mexican Tropical Dry Forest1

We evaluated the temporal and spatial patterns of abundance and the amount of damage caused by gall‐inducing insects (GII) in deciduous and riparian habitats in a seasonal tropical dry forest in Mexico. Plants occurring in these habitats differ in their phenology and moisture availability. Deciduous habitats are seasonal and xeric, while riparian habitats are aseasonal and mesic. We found 37 GII species and each one was associated with a specific plant species. In total, 19 species (51.3%) were present in deciduous habitats, 13 species (35.2%) in riparian habitats, and only 5 species (13.5%) occurred in both. Abundance and leaf damage by GII were greater in deciduous than in riparian habitats during the wet season. For each GII species that occurred in both habitats, host plant species supported greater abundance and leaf damage by GII in deciduous habitats during the wet season. These results indicate a greater association of GII species with host plants in deciduous than in riparian habitats during the wet season. In riparian habitats, 11 plant species (61.1%) had greater density of GII in the dry than in the wet season. Similarly, leaf damage by GII was significantly greater in the dry than in the wet season in riparian habitats for 12 plant species (66.7%). Dry forest plants of riparian habitats presented two peaks of leaf‐flushing: GII colonized leaves produced in the first peak at the beginning of the wet season, and accumulated or recolonized leaves in the second peak at the beginning of the dry season. The levels of leaf damage by GII detected in this study in the rainy season were considerably higher than those obtained for folivorous insects in other neotropical forests, suggesting that this GII guild might have an important impact on their host plant species in this tropical community.     

Snowshoe hares display limited phenotypic plasticity to mismatch in seasonal camouflage

As duration of snow cover decreases owing to climate change, species undergoing seasonal colour moults can become colour mismatched with their background. The immediate adaptive solution to this mismatch is phenotypic plasticity, either in phenology of seasonal colour moults or in behaviours that reduce mismatch or its consequences. We observed nearly 200 snowshoe hares across a wide range of snow conditions and two study sites in Montana, USA, and found minimal plasticity in response to mismatch between coat colour and background. We found that moult phenology varied between study sites, likely due to differences in photoperiod and climate, but was largely fixed within study sites with only minimal plasticity to snow conditions during the spring white-to-brown moult. We also found no evidence that hares modify their behaviour in response to colour mismatch. Hiding and fleeing behaviours and resting spot preference of hares were more affected by variables related to season, site and concealment by vegetation, than by colour mismatch. We conclude that plasticity in moult phenology and behaviours in snowshoe hares is insufficient for adaptation to camouflage mismatch, suggesting that any future adaptation to climate change will require natural selection on moult phenology or behaviour.     

Cool habitats support darker and bigger butterflies in Australian tropical forests

Morphology mediates the relationship between an organism's body temperature and its environment. Dark organisms, for example, tend to absorb heat more quickly than lighter individuals, which could influence their responses to temperature. Therefore, temperature‐related traits such as morphology may affect patterns of species abundance, richness, and community assembly across a broad range of spatial scales. In this study, we examined variation in color lightness and body size within butterfly communities across hot and cool habitats in the tropical woodland–rainforest ecosystems of northeast Queensland, Australia. Using thermal imaging, we documented the absorption of solar radiation relative to color lightness and wingspan and then built a phylogenetic tree based on available sequences to analyze the effects of habitat on these traits within a phylogenetic framework. In general, darker and larger individuals were more prevalent in cool, closed‐canopy rainforests than in immediately adjacent and hotter open woodlands. In addition, darker and larger butterflies preferred to be active in the shade and during crepuscular hours, while lighter and smaller butterflies were more active in the sun and midday hours—a pattern that held after correcting for phylogeny. Our ex situ experiment supported field observations that dark and large butterflies heated up faster than light and small butterflies under standardized environmental conditions. Our results show a thermal consequence of butterfly morphology across habitats and how environmental factors at a microhabitat scale may affect the distribution of species based on these traits. Furthermore, this study highlights how butterfly species might differentially respond to warming based on ecophysiological traits and how thermal refuges might emerge at microclimatic and habitat scales.     

丝带凤蝶滞育与非滞育蛹及其成虫的形态学观察

丝带凤蝶Sericinus montelus是一种有开发价值的观赏昆虫,以蛹滞育越冬,成虫存在多型现象。本研究从体色、个体大小和蛹腹部刺突长度等方面比较了丝带凤蝶滞育与非滞育蛹及其成虫的形态差异。与非滞育蛹相比,滞育蛹体色较深,触角末端的淡黄色与体色差异明显,3日龄滞育蛹腹部第9节刺突长度是3日龄非滞育蛹的4倍左右,这些差异可以用于该虫蛹滞育早期判别。滞育蛹羽化成虫的翅展和尾突长度显著小于非滞育蛹羽化成虫,且腹部及翅面斑纹也存在明显的差异,这些差异与丝带凤蝶春型、夏型成虫的描述相一致,表明丝带凤蝶成虫季节多型是与滞育相关联的。     

‘Stick with your own kind,or hang with the locals?’ Implications of shoaling strategy for tropical reef fish on a range‐expansion frontline

Range shifts of tropical marine species to temperate latitudes are predicted to increase as a consequence of climate change. To date, the research focus on climate‐mediated range shifts has been predominately dealt with the physiological capacity of tropical species to cope with the thermal challenges imposed by temperate latitudes. Behavioural traits of individuals in the novel temperate environment have not previously been investigated, however, they are also likely to play a key role in determining the establishment success of individual species at the range‐expansion forefront. The aim of this study was to investigate the effect of shoaling strategy on the performance of juvenile tropical reef fishes that recruit annually to temperate waters off the south east coast of Australia. Specifically, we compared body‐size distributions and the seasonal decline in abundance through time of juvenile tropical fishes that shoaled with native temperate species (‘mixed’ shoals) to those that shoaled only with conspecifics (as would be the case in their tropical range). We found that shoaling with temperate native species benefitted juvenile tropical reef fishes, with individuals in ‘mixed’ shoals attaining larger body‐sizes over the season than those in ‘tropical‐only’ shoals. This benefit in terms of population body‐size distributions was accompanied by greater social cohesion of ‘mixed’ shoals across the season. Our results highlight the impact that sociality and behavioural plasticity are likely to play in determining the impact on native fish communities of climate‐induced range expansion of coral reef fishes.     

The conceptual and practical implications of interpreting diet breadth mechanistically in generalist predatory insects

Seasonal polyphenism in animal colour patterns indicates that temporal variation in selection pressures maintains phenotypic plasticity. Spring generation of the polyphenic European map butterfly Araschnia levana has an orange–black fritillary‐like pattern whilst individuals of the summer generation are black with white bands across the wings. What selects for the colour difference is unknown. Because predation is a major selection pressure for insect coloration, we first tested whether map butterfly coloration could have a warning function (i.e. whether the butterflies are unpalatable to birds). In a following field experiment with butterfly dummies we tested whether the spring form is better protected than the summer form from predators in the spring, and vice versa in the summer. The butterflies were palatable to birds (blue tits Cyanistes caeruleus) and in the field the spring and summer form dummies were attacked equally irrespective of season. Therefore, we found no evidence that the map butterfly is warning‐coloured or that seasonal polyphenism is an adaptation to avian predation. Because insect coloration has multiple functions and map butterfly coloration is linked to morphology, life history and development it is likely that the interplay of several selection pressures explains the evolution of colour polyphenism. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.     

Is seasonal variation in leaf traits adaptive for the annual plant Dicerandra linearifolia?

Empirical studies of phenotypic plasticity have often relied on the plausibility that a plastic response to the environment would increase fitness in order to diagnose the response as adaptive. I conducted a test of the hypothesis that seasonal variation in leaf traits is an adaptive response to seasonal variation in environmental conditions faced by the annual plant Dicerandralinearifolia. This species exhibits variation in leaf morphology and anatomy in response to temperature that is consistent with the expectations for adaptive plasticity. I examined variation in the size, thickness and density of stomata of leaves that develop in summer and winter and used analysis of phenotypic selection during winter and summer seasons to test the hypothesis that seasonal variation in these traits is adaptive. Regression analyses of estimated dry mass (as a proxy for fitness) on leaf traits revealed no evidence supporting the adaptive hypothesis. Selection favoured individuals with large and thick leaves in both winter and summer, and density of stomata had little or no effect on estimated relative fitness in any season. Correspondence between seasonal variation in leaf thickness and density of stomata and expectations for adaptive plasticity appears to be purely fortuitous. Seasonal variation in leaf traits may persist simply because there is no selection against individuals in which these traits vary. My results underscore the importance of definitive tests of the hypothesis of adaptation to distinguish adaptive plasticity from neutral or nonadaptive phenotypic plasticity.     

Expression of alternative developmental pathways in the cabbage butterfly,Pieris melete and their differences in life history traits

The seasonal life cycle of the cabbage butterfly, Pieris melete is complicated because there are three options for pupal development: summer diapause, winter diapause, and nondiapause. In the present study, we tested the influence of temperature, day length, and seasonality on the expression of alternative developmental pathways and compared the differences in life history traits between diapausing and directly developing individuals under laboratory and field conditions. The expression of developmental pathway strongly depended on temperature, day length, and seasonality. Low temperatures induced almost all individuals to enter diapause regardless of day length; relatively high temperatures combined with intermediate and longer day lengths resulted in most individuals developing without diapause in the laboratory. The field data revealed that the degree of phenotypic plasticity in relation to developmental pathway was much higher in autumn than in spring. Directly developing individuals showed shorter development times and higher growth rates than did diapausing individuals. The pupal and adult weights for both diapausing and directly developing individuals gradually decreased as rearing temperature increased, with the diapausing individuals being slightly heavier than the directly developing individuals at each temperature. Female body weight was slightly lower than male body weight. The proportional weight losses from pupa to adult were almost the same in diapausing individuals and in directly developing individuals, suggesting that diapause did not affect weight loss at metamorphosis. Our results highlight the importance of the expression of alternative developmental pathways, which not only synchronizes this butterfly's development and reproduction with the growth seasons of the host plants but also exhibits the bet‐hedging tactic against unpredictable risks due to a dynamic environment.     

Seasonal androgen cycles in adult male American alligators (Alligator mississippiensis) from a barrier island population

The seasonal patterns of two primary plasma androgens, testosterone (T) and dehydroepiandrosterone (DHEA), were assessed in adult male alligators from the Merritt Island National Wildlife Refuge, a unique barrier island environment and home to the Kennedy Space Center in Florida. Samples were collected monthly from 2008 to 2009, with additional samples collected at more random intervals in 2007 and 2010. Plasma T concentrations peaked in April, coincident with breeding and courtship, and declined rapidly throughout the summer. Seasonal plasma T patterns in smaller though reproductively active adult males differed from those in their larger counterparts during the breeding season. Both size classes showed significant increases in plasma T concentration from February to March, at the beginning of the breeding season. However, smaller adults did not experience the peak in plasma T concentrations in April that were observed in larger adults, and their concentrations were significantly lower than those of larger males for the remainder of the breeding season. Plasma DHEA concentrations peaked in May and were significantly reduced by June. This is the first study to demonstrate the presence of DHEA in a crocodilian, and the high plasma DHEA concentrations that paralleled the animals' reproductive activity suggest a reproductive and/or behavioral role in adult male alligators. Similar to androgen variations in some birds, plasma DHEA concentrations in the alligators were considerably higher than T concentrations during the nonbreeding season, suggesting a potential role in maintaining nonbreeding seasonal aggression.     

黑带食蚜蝇体色变异的研究

通过对黑带食蚜蝇Episyrphus balteatus(De Geer)体色变异的研究,发现黑带食蚜蝇存在深色型和浅色型2种基本形式,体色变异具有明显的季节性,深色型个体出现在温度较低的秋季及早春,浅色型个体发生在温度较高的春夏季节;在腹部色斑方面,深色型和浅色型个体中均存在变异,可划分为8种类型,腹部色斑的变异在浅色型个体中较为丰富,腹部不同体节背板上色斑的变异程度不同;黑带食蚜蝇在体型大小方面同样存在差异,这些变异的多态性可能是食蚜蝇系统学研究中异名产生的一个重要原因。因此,食蚜蝇类群的个体体色变异在系统学研究中是一个必须特别注意的问题。