Effects of hatching age on development and hatchling morphology in the red-eyed tree frog, Agalychnis callidryas

The red-eyed treefrog, Agalychnis callidryas , lays eggs on leaves overhanging ponds. Tadpoles hatch and enter the water at different ages, and late-hatched tadpoles survive aquatic predators better than do early-hatched tadpoles. Here I assess developmental consequences of hatching age through: (1) a morphological study of embryos and tadpoles through the plastic hatching period; (2) a behavioural assay for an effect of hatching age on feeding; and (3) a field experiment testing the effect of hatching age on growth to metamorphosis. Substantial development of feeding, digestive, respiratory and locomotor structures occurs in embryos over the plastic hatching period. Hatchling morphology thus varies with age, with consequences for behaviour and predation risk. Hatched tadpoles develop faster than embryos, and early-hatched tadpoles feed before late-hatched tadpoles. After all tadpoles have hatched, the effect of hatching age on size decreases. I found no evidence for an effect of hatching age on size at metamorphosis and only weak evidence for an effect on larval period. Hatching age affects the sequence of developmental change: early-hatched tadpoles lose external gills while otherwise more developed embryos maintain them. Plasticity in external gill resorption may be adaptive given differences in the respiratory environments of embryos and tadpoles. Early-hatched tadpoles also diverge from embryos in shape, growing relatively smaller tails. The study of functional morphology and developmental plasticity will contribute to understanding hatching as an ontogenetic niche shift.     

Physiological,Behavioral and Maternal Factors That Contribute to Size Variation in Larval Amphibian Populations

Size variance among similarly aged individuals within populations is a pattern common to many organisms that is a result of interactions between intrinsic and extrinsic traits of individuals. While genetic and maternal effects, as well as physiological and behavioral traits have been shown to contribute to size variation in animal populations, teasing apart the influence of such factors on individual growth rates remain a challenge. Furthermore, tracing the effects of these interactions across life stages and in shaping adult phenotypes also requires further exploration. In this study we investigated the relationship between genetics, hatching patterns, behaviors, neuroendocrine stress axis activity and variance in growth and metamorphosis among same-aged larval amphibians. Through parallel experiments we found that in the absence of conspecific interactions, hatch time and to a lesser extent egg clutch identity (i.e. genetics and maternal effects) influenced the propensity for growth and development in individual tadpoles and determined metamorphic traits. Within experimental groups we found that variance in growth rates was associated with size-dependent foraging behaviors and responses to food restriction. We also found an inverse relationship between glucocorticoid (GC) hormone levels and body mass and developmental stage among group-reared tadpoles, which suggests that GC expression plays a role in regulating differing within-population growth trajectories in response to density-dependent conditions. Taken together these findings suggest that factors that influence hatching conditions can have long-term effects on growth and development. These results also raise compelling questions regarding the extent to which maternal and genetic factors influence physiological and behavioral profiles in amphibians.     

Risk‐induced hatching timing shows low heritability and evolves independently of spontaneous hatching in red‐eyed treefrogs

Plasticity in the timing of transitions between stages of complex life cycles allows organisms to adjust their growth and development to local environmental conditions. Genetic variation in such plasticity is common, but the evolution of context‐dependent transition timing may be constrained by information reliability, lag‐time and developmental constraints. We studied the genetic architecture of hatching plasticity in embryos of the red‐eyed treefrog (Agalychnis callidryas) in response to simulated predator attacks using a series of paternal and maternal half‐sibs from a captive breeding colony of wild‐collected animals. We compared the developmental timing of induced early hatching across sibships and estimated cross‐environment genetic correlations between induced and spontaneous hatching traits. Additive genetic variance for induced early hatching was very low, indicating a constraint on the short‐term evolution of earlier hatching timing. This constraint is likely related to the maturation of the hatching mechanism. The most plastic genotypes produced the most extreme spontaneous hatching phenotypes, indicating that developmental range, per se, is not constrained. Cross‐environment genetic correlation in hatching timing was negligible, so the evolution of spontaneous hatching in this species has not depended on the evolution of risk‐induced hatching and vice versa.     

Life-history variation in relation to time constraints in a damselfly

Although variation within populations in plasticity to time constraints is expected with regard to hatching date, empirical studies are largely lacking. We studied life-history responses to time constraints manipulated by photoperiod and associated with hatching date in larvae of the damselfly Lestes viridis for two populations with a different hydroperiod. In a common garden experiment, early- and late-hatched larvae from both populations were reared at two photoperiods mimicking the start and the end of the egg-hatching season. In a reciprocal transplant experiment, early- and late-hatched larvae from both populations were reared in both ponds. In all these experiments, larvae were reared from egg hatching until adult emergence. Within both populations, larvae reared at the photoperiod indicating a late time point in the growing season, reduced development time to compensate for their perceived shorter development period. Growth rate, however, did not respond to photoperiod, resulting in a lower mass at emergence. As expected, both in the laboratory and in the field, larvae from eggs that hatched later in the season generally had a shorter development time and a faster growth rate, resulting in a higher mass at emergence compared to early-hatched larvae. This may explain the intriguing seasonal increase in mass at emergence in this species, and affect the predictions of optimality models. None of these life-history responses differed between the two populations, despite clear differences in time constraints linked to hydroperiod, suggesting the robustness of the observed patterns. Given the ubiquity of asynchronous hatching in nature, and the adaptive value of the observed differences between early- and late-hatched larvae, we expect the effects of hatching date on life-history plasticity to be widespread.     

Oxygen, gills, and embryo behavior: mechanisms of adaptive plasticity in hatching.

Many species alter the timing of hatching in response to egg or larval predators, pathogens, or physical risks. This plasticity depends on separation between the onset of hatching competence and physiological limits to embryonic development. I present a framework based on heterokairy to categorize developmental mechanisms and identify traits contributing to and limiting hatching plasticity, then apply it to a case of predator-induced hatching. Red-eyed treefrogs have arboreal eggs, and tadpoles fall into ponds upon hatching. Egg and tadpole predators select for earlier and later hatching, respectively. Embryos hatch up to 30% early in predator attacks, and later if undisturbed. They maintain large external gills throughout the plastic hatching period, delaying gill regression while development otherwise continues. Rapid gill regression occurs upon hatching. Prolonged embryonic development depends on external gills; inducing gill regression causes hatching. External hypoxia retards development, kills eggs, and induces hatching. Nonetheless, embryos develop synchronously and without hatching prematurely across a broad range of perivitelline PO2, from 0.5-12.5 kPa. Embryos exploit spatial variation of PO2 within eggs by positioning gills against patches of air-exposed surface. Respiratory plasticity and oxygen-sensitive behavior appear critical for the hatching plasticity that balances a predation risk trade-off across life stages.     

Oxygen, gills, and embryo behavior: mechanisms of adaptive plasticity in hatching

Many species alter the timing of hatching in response to egg or larval predators, pathogens, or physical risks. This plasticity depends on separation between the onset of hatching competence and physiological limits to embryonic development. I present a framework based on heterokairy to categorize developmental mechanisms and identify traits contributing to and limiting hatching plasticity, then apply it to a case of predator-induced hatching. Red-eyed treefrogs have arboreal eggs, and tadpoles fall into ponds upon hatching. Egg and tadpole predators select for earlier and later hatching, respectively. Embryos hatch up to 30% early in predator attacks, and later if undisturbed. They maintain large external gills throughout the plastic hatching period, delaying gill regression while development otherwise continues. Rapid gill regression occurs upon hatching. Prolonged embryonic development depends on external gills; inducing gill regression causes hatching. External hypoxia retards development, kills eggs, and induces hatching. Nonetheless, embryos develop synchronously and without hatching prematurely across a broad range of perivitelline PO₂, from 0.5–12.5 kPa. Embryos exploit spatial variation of PO₂ within eggs by positioning gills against patches of air-exposed surface. Respiratory plasticity and oxygen-sensitive behavior appear critical for the hatching plasticity that balances a predation risk trade-off across life stages.     

Pre-hatching exposure to water mold reduces size at metamorphosis in the moor frog

Developmental plasticity is increasingly recognized as important for ecological and evolutionary processes. However, few studies consider the potential for delayed effects of early environments. Here, we show that tadpoles hatching from clutches exposed to water mold (Saprolegnia) have 20% decreased mass at metamorphosis, despite no further exposure subsequent to hatching. The effects were consistent across four populations that have previously been shown to vary in their resistance to infection during embryonic development. Contrary to expectations, time to hatching or metamorphosis was not affected, suggesting that the results do not reflect an evolved escape strategy from infected waters triggered by embryonic conditions. Instead, decreased mass at metamorphosis may arise from carry-over effects of impaired embryo development. Such strong links across developmental stages have potential consequences for the evolution of plasticity and the responses of populations to emergent infections.     

Seasonal variation in growth of greater snow goose goslings: the role of food supply

Even though growth rate is an important fitness component, it is still controversial to what extent parent birds adjust the timing of offspring hatch to natural variations in food supply to maximize offspring growth. We studied the role of food availability in explaining inter- and intra-seasonal variation of growth rate in goslings of greater snow geese over 5 years. The peak of hatching generally coincided with the peak of food availability. However, early-hatched goslings usually grew faster than birds hatched at the peak, which in␣turn grew faster than late-hatched goslings, although this phenomenon was not observed in all years. There was considerable variation in growth rate among the five years, the smallest goslings produced in the best year (1991) being larger than the largest goslings of the poorest year (1994). We developed three indices of food availability, based on the cumulative availability of plant biomass and nitrogen content during the growth period, and showed that the cumulative exposure to nitrogen biomass explained up to 43% of variation (intra- and inter-annual) in body size just before fledging. In years with good feeding conditions, early-hatched goslings had access to more nitrogen during their growing period than those hatching on or after the peak and they grew faster. In years of lower food availability, early-hatched goslings had no detectable advantage over peak- or late-hatched birds for access to protein-rich food and no seasonal decline in growth rate was observed. These results confirm the critical role of food supply in the seasonal variation of growth rate in Arctic-nesting geese. Received: 27 June 1997 / Accepted: 9 October 1997     

Environmental context shapes immediate and cumulative costs of risk-induced early hatching

In animals with complex life cycles, fitness trade-offs across life stages determine the optimal time for transitions between stages. If these trade-offs vary predictably, adaptive plasticity in the timing of life history transitions may evolve. For instance, embryos of many species are capable of accelerating hatching to escape from egg predation and other hazards, but for plasticity in hatching timing to be selectively maintained, early hatching must also entail costs, probably in subsequent life stages. However the post-hatching environment, which influences this cost, is variable in nature. We assessed how two elements of the post-hatching environment, predator species and age structure created by hatching age plasticity, affect costs of hatching early in red-eyed treefrogs, Agalychnis callidryas. Red-eyed treefrog embryos were induced to hatch at the onset of hatching competence or near the peak of spontaneous hatching and exposed to one of three insect predators in single or mixed hatching-age treatments. Age structure created by hatching-age plasticity did not affect tadpole survivorship or growth; however, the consequences of hatching timing depended on predator species and foraging mode. Tadpoles that were induced to hatch early experienced initially higher mortality rates only with the more actively foraging predator. Nonetheless, mortality costs of accelerated hatching were apparent with all predators once we factored in the longer duration of exposure that early hatchlings experience in nature. This study suggests that extended exposure of young larvae to predators may be a general cost of early hatching, explaining why spontaneous hatching occurs later in life across variable environmental contexts.     

WHY ONTOGENY MATTERS DURING ADAPTATION: DEVELOPMENTAL NICHE CONSTRUCTION AND PLEIOTORPY ACROSS THE LIFE CYCLE IN ARABIDOPSIS THALIANA

This case study of adaptation in Arabidopsis thaliana shows that natural selection on early life stages can be intense and can influence the evolution of subsequent traits. Two mechanisms contribute to this influence: pleiotropy across developmental stages and developmental niche construction. Examples are given of pleiotropy of environmentally cued development across life stages, and potential ways that pleiotropy can be relieved are discussed. In addition, this case study demonstrates how the timing of prior developmental transitions determines the seasonal environment experienced subsequently, and that such developmental niche construction alters phenotypic expression of subsequent traits, the expression of genetic variation of those traits, and natural selection on those traits and alleles associated with them. As such, developmental niche construction modifies pleiotropic relationships across the life cycle in ways that influence the dynamics of adaptation. Understanding the genetic basis of life‐cycle variation therefore requires consideration of environmental effects on pleiotropy.     

Experimental evolution of bet hedging in rotifer diapause traits as a response to environmental unpredictability

The adaptive response of organisms to unpredictable environments is increasingly recognized as a central topic in fundamental and applied evolutionary ecology. Selection due to environmental unpredictability can act on multiple traits of an organism's life cycle to reduce the impact of high environmental variance. The aim of this research was to study how unpredictability selects for diapause traits: 1) the timing of sex (a proxy of the timing of diapausing egg production), and 2) the diapausing egg hatching fraction (a proxy of diapause duration). We used an experimental evolution approach with the facultative sexual rotifer Brachionus plicatilis. Laboratory populations experiencing two contrasting regimes of environmental fluctuation (predictable versus unpredictable) evolved divergently over a short time span (< 77 days). The populations under the unpredictable regime showed an earlier initiation of sexual reproduction and a lower hatching fraction of diapausing eggs than populations under the predictable regime. These findings demonstrate empirically the existence of bet‐hedging strategies in B. plicatilis regarding both traits, consistent with theoretical predictions of bet‐hedging evolution under conditions of unpredictable environmental variance. Given that scenarios of increased environmental variability are expected to occur in the near future, a comprehensive understanding of the role of bet‐hedging strategies is necessary for predicting population responses to environmental change.     

The genetics of adaptation to novel environments: selection on germination timing in Arabidopsis thaliana

When studying selection during adaptation to novel environments, researchers have often paid little attention to an organism’s earliest developmental stages. Despite this lack of attention, early life history traits may be under strong selection during colonization, as the expression of adaptive phenotypes at later points is contingent upon early survival. Moreover, the timing of early developmental transitions can constrain the timing of later transitions, with potentially large effects on fitness. In this issue, Huang et al. (2010) underscore the importance of early life history traits in the adaptation of Arabidopsis thaliana to old‐field sites in North America. Using a new population of mapped recombinant inbred lines, the authors examined germination timing and total lifetime fitness of A. thaliana while varying site latitude, dispersal season, and maternal photoperiod. Huang et al. (2010) discovered several Quantitative Trait Loci (QTL) with large effects on fitness that colocalized with QTL for field germination timing and seed dormancy—demonstrating that fitness is genetically associated with these early life history traits, and that these loci are likely under strong selection during adaptation to novel environments. In the epistatic interactions of some loci, recombinant genotypes outperformed parental genotypes, supporting the potentially adaptive role of recombination. This study provides elegant evidence that traits expressed early in an organism’s development can play an important role during adaptive evolution.     

Alternative development in Polystoma gallieni (Platyhelminthes,Monogenea) and life cycle evolution

Considering the addition of intermediate transmission steps during life cycle evolution, developmental plasticity, canalization forces and inherited parental effect must be invoked to explain new host colonization. Unfortunately, there is a lack of experimental procedures and relevant models to explore the adaptive value of alternative developmental phenotypes during life cycle evolution. However, within the monogeneans that are characterized by a direct life cycle, an extension of the transmission strategy of amphibian parasites has been reported within species of Polystoma and Metapolystoma (Polyopisthocotylea; Polystomatidae). In this study, we tested whether the infection success of Polystoma gallieni within tadpoles of its specific host, the Stripeless Tree Frog Hyla meridionalis, differs depending on the parental origin of the oncomiracidium. An increase in the infection success of the parasitic larvae when exposed to the same experimental conditions as their parents was expected as an adaptive pattern of non-genetic inherited information. Twice as many parasites were actually recorded from tadpoles infected with oncomiracidia hatching from eggs of the bladder parental phenotype (1.63 ± 0.82 parasites per host) than from tadpoles infected with oncomiracidia hatching from eggs of the branchial parental phenotype (0.83 ± 0.64 parasites per host). Because in natural environments the alternation of the two phenotypes is likely to occur due to the ecology of its host, the differential infection success within young tadpoles could have an adaptive value that favors the parasite transmission over time.     

When and how can <Emphasis Type="Italic">Daphnia</Emphasis> prepare their offspring for the threat of predation?

The life history of Daphnia exposed to fish kairomone at different developmental stages was examined in a laboratory experiment. The strongest life history response to the applied predation threat was observed in females exposed during the 4th instar. Compared to Daphnia experiencing the presence of fish at earlier or later instars, these individuals reached maturity at a smaller size and released fewer neonates. Moreover, their offspring also demonstrated the strongest reaction to predation threat, exhibiting the broadest phenotypic plasticity in the life history response to predation. The breadth of their reaction norm was, on average, two times larger comparing with individuals from other treatments. Broader phenotypic plasticity may offer clear selective advantages under the unpredictable predation regime. This finding highlights the adaptive role of maternal effect in shaping life history of cladocerans.     

The thrifty phenotype as an adaptive maternal effect

Human diseases in adulthood are increasingly associated with growth patterns in early life, implicating early-life nutrition as the underlying mechanism. The thrifty phenotype hypothesis proposed that early-life metabolic adaptations promote survival, with the developing organism responding to cues of environmental quality by selecting an appropriate trajectory of growth. Recently, some authors have proposed that the thrifty phenotype is also adaptive in the longer-term, by preparing the organism for its likely adult environment. However, windows of plasticity close early during human development, and subsequent environmental changes may result in the selected trajectory becoming inappropriate, leading to adverse effects on health. This paradox generates uncertainty as to whether the thrifty phenotype is indeed adaptive for the offspring in humans. The thrifty phenotype should not be considered a dichotomous concept, rather it refers to the capacity of all offspring to respond to environmental information during early ontogenetic development. This article argues that the thrifty phenotype is the consequence of three different adaptive processes - niche construction, maternal effects, and developmental plasticity - all of which in humans are influenced by our large brains. While developmental plasticity represents an adaptation by the offspring, both niche construction and parental effects are subject to selection on parental rather than offspring fitness. The three processes also operate at different paces. Human offspring do not become net calories-producers until around 18 years of age, such that the high energy costs of the human brain are paid primarily by the mother, even after weaning. The evolutionary expansion of human brain volume occurred in environments characterised by high volatility, inducing strong selective pressure on maternal capacity to provision multiple offspring simultaneously. The thrifty phenotype is therefore best considered as a manipulation of offspring phenotype for the benefit of maternal fitness. The information that enters offspring phenotype during early development does not predict the likely future environment of the offspring, but rather reflects the mother's own developmental experience and the quality of the environment during her own maturation. Offspring growth trajectory thus becomes aligned with long-term maternal capacity to provision. In contemporary populations, the sensitivity of offspring development to maternal phenotype exposes the offspring to adverse effects, through four distinct pathways. The offspring may be exposed to (1) poor maternal metabolic control (e.g. gestational diabetes), (2) maternally derived toxins (e.g. maternal smoking), or (3) low maternal social status (e.g. small size). Adverse consequences of these effects may then be exacerbated by (4) exposure either to the "toxic" western environment in postnatal life, in which diet and physical activity levels are mismatched with metabolic experience in utero, or at the other extreme to famine. The rapid emergence of the epidemic of the metabolic syndrome in the 20th Century reflects the rapid acceleration in the pace of niche construction relative to the slower physiological combination of developmental plasticity and parental effects.     

Effects of food restriction across stages of juvenile and early adult development on body weight,survival and adult life history

Organisms have to allocate limited resources among multiple life‐history traits, which can result in physiological trade‐offs, and variation in environmental conditions experienced during ontogeny can influence reproduction later in life. Food restriction may lead to an adaptive reallocation of the limited resources among traits as a phenotypically plastic adjustment, or it can act as an overall constraint with detrimental effects throughout reproductive life. In this study, we investigated experimentally the effects of food restriction during different stages of the juvenile and early adult development on body weight, survival and reproductive success in females and males of the European earwig Forficula auricularia. Individuals either received limited or unlimited access to food across three different stages of development (fully crossed) allowing us to identify sensitive periods during development and to test both additive and interactive effects of food limitation across stages on development and reproduction. Food restriction during the early and late juvenile stage had additive negative effects on juvenile survival and adult body weight. With regard to reproductive success of females which produce up to two clutches in their lifetime, restriction specifically in the late juvenile stage led to smaller first and second clutch size, lower probability of second clutch production and reduced hatching success in the second clutch. Reproductive success of females was not significantly affected when their male mates experienced food restriction during their development. Our findings in general support the ‘silver‐spoon’ hypothesis in that food restriction during juvenile development poses constraints on development and reproduction throughout life.     

INTERACTIVE EFFECTS OF OFFSPRING SIZE AND TIMING OF REPRODUCTION ON OFFSPRING REPRODUCTION: EXPERIMENTAL,MATERNAL, AND QUANTITATIVE GENETIC ASPECTS

We demonstrate that egg size in side-blotched lizards is heritable (parent-offspring regressions) and thus will respond to natural selection. Because our estimate of heritability is derived from free-ranging lizards, it is useful for predicting evolutionary response to selection in wild populations. Moreover, our estimate for the heritability of egg size is not likely to be confounded by nongenetic maternal effects that might arise from egg size per se because we estimate a significant parent-offspring correlation for egg size in the face of dramatic experimental manipulation of yolk volume of the egg. Furthermore, we also demonstrate a significant correlation between egg size of the female parent and clutch size of her offspring. Because this correlation is not related to experimentally induced maternal effects, we suggest that it is indicative of a genetic correlation between egg size and clutch size. We synthesize our results from genetic analyses of the trade-off between egg size and clutch size with previously published experiments that document the mechanistic basis of this trade-off. Experimental manipulation of yolk volume has no effect on offspring reproductive traits such as egg size, clutch size, size at maturity, or oviposition date. However, egg size was related to offspring survival during adult phases of the life history. We partitioned survival of offspring during the adult phase of the life history into (1) survival of offspring from winter emergence to the production of the first clutch (i.e., the vitellogenic phase of the first clutch), and (2) survival of the offspring from the production of the first clutch to the end of the reproductive season. Offspring from the first clutch of the reproductive season in the previous year had higher survival during vitellogenesis of their first clutch if these offspring came from small eggs. We did not observe selection during these prelaying phases of adulthood for offspring from later clutches. However, we did find that later clutch offspring from large eggs had the highest survival over the first season of reproduction. The differences in selection on adult survival arising from maternal effects would reinforce previously documented selection that favors the production of small offspring early in the season and large offspring later in the season—a seasonal shift in maternal provisioning. We also report on a significant parent-offspring correlation in lay date and thus significant heritable variation in lay date. We can rule out the possibility of yolk volume as a confounding maternal effect—experimental manipulation of yolk volume has no effect on lay date of offspring. However, we cannot distinguish between genetic effects (i.e., heritable) and nongenetic maternal effects acting on lay date that arise from the maternal trait lay date per se (or other unidentified maternal traits). Nevertheless, we demonstrate how the timing of female reproduction (e.g., date of oviposition and date of hatching) affect reproductive attributes of offspring. Notably, we find that date of hatching has effects on body size at maturity and fecundity of offspring from later clutches. We did not detect comparable effects of lay date on offspring from the first clutch.     

Hatching late in the season requires flexibility in the timing of song learning

Most songbirds learn their songs from adult tutors, who can be their father or other male conspecifics. However, the variables that control song learning in a natural social context are largely unknown. We investigated whether the time of hatching of male domesticated canaries has an impact on their song development and on the neuroendocrine parameters of the song control system. Average age difference between early- and late-hatched males was 50 days with a maximum of 90 days. Song activity of adult tutor males decreased significantly during the breeding season. While early-hatched males were exposed to tutor songs for on average the first 99 days, late-hatched peers heard adult song only during the first 48 days of life. Remarkably, although hatching late in the season negatively affected body condition, no differences between both groups of males were found in song characteristics either in autumn or in the following spring. Similarly, hatching date had no effect on song nucleus size and circulating testosterone levels. Our data suggest that late-hatched males must have undergone accelerated song development. Furthermore, the limited tutor song exposure did not affect adult song organization and song performance.     

Phenotypic Variations in the Life History of Two Clones of Macrobiotus richtersi (Eutardigrada, Macrobiotidae)

A comparative study of life history traits of two clones (CDMr01 and CDMr02) of a triploid thelytokous apomictic population of the eutardigrade Macrobiotus richtersi has been carried out. Both clones were reared under the same lab conditions: temperature of 14 °C, photoperiod of 12 h/12 h (L/D), and nematodes ad libitum as food. Statistical analysis of the life history traits considered has indicated interclonal variability. The two clones were significantly different in the number of eggs per clutch (fertility), number of eggs laid per female per life span (fecundity), hatching percentage of eggs and hatching time. Similarities between clones have been observed with regard to life span, total number of ovipositions per life span, and age at first oviposition. In addition, significant differences in hatching time, with eggs hatched over a long period, were found within each clone. Interclonal variability in life history traits indicated the effects of genetic factors, whereas intraclonal variability reflected the effects of environmental factors. The evolutionary and adaptive significance of the life history phenotypic variations is discussed.     

Environmentally cued hatching across taxa: embryos respond to risk and opportunity

Most animals begin life in eggs, protected and constrained by a capsule, shell, or other barrier. As embryos develop, their needs and abilities change, altering the costs and benefits of encapsulation, and the risks and opportunities of the outside world. When the cost/benefit ratio is better outside the egg, animals should hatch. Adaptive timing of hatching evolves in this context. However, many environmental variables affect the optimal timing of hatching so there is often no consistent best time. Across a broad range of animals, from flatworms and snails to frogs and birds, embryos hatch at different times or at different developmental stages in response to changing risks or opportunities. Embryos respond to many types of cues, assessed via different sensory modalities. Some responses appear simple. Others are surprisingly complex and sophisticated. Parents also manipulate the timing of hatching. The number and breadth of examples of cued hatching suggest that, in the absence of specific information, we should not assume that hatching timing is fixed. Our challenge now is to integrate information on the timing of hatching across taxa to better understand the diversity of patterns and how they are structured in relation to different types of environmental and developmental variation. As starting points for comparative studies, I: (1) suggest a framework based on heterokairy-individual, plastic variation in the rate, timing, or sequence of developmental events and processes-to describe patterns and mechanisms of variation in the timing of hatching; (2) briefly review the distribution of environmentally cued hatching across the three major clades of Bilateria, highlighting the diverse environmental factors and mechanisms involved; and (3) discuss factors that shape the diversity of plastic and fixed timing of hatching, drawing on evolutionary theory on phenotypic plasticity which directs our attention to fitness trade-offs, environmental heterogeneity, and predictive cues. Combining mechanistic and evolutionary perspectives is necessary because development changes organismal interactions with the environment. Integrative and comparative studies of the timing of hatching will improve our understanding of embryos as both evolving and developing organisms.