Model systems in developmental biology

The practical criteria by which developmental biologists choose their model systems have evolutionary correlates. The result is a sample that is not merely small, but biased in particular ways, for example towards species with rapid, highly canalized development. These biases influence both data collection and interpretation, and our views of how development works and which aspects of it are important.     

Maximum titers of vitellogenin and total hemolymph protein occur during the canalized phase of grasshopper egg production.

Many organisms exhibit developmental plasticity only in sensitive phases and cannot respond to environmental perturbations at other times. However, we know little about the physiological events that define plastic and canalized phases. During egg production in insects, vitellogenin (Vg) accumulates first in the hemolymph and then in the eggs. In addition, storage proteins may be important resources for egg production. Therefore, we tested hypotheses on the relationships of Vg and TP (total hemolymph protein minus Vg) titers to the transition from flexible to inflexible development during egg production. In lubber grasshoppers, approximately 70% of TP is contained in three proteins that range from 68 to 83 kDa. We maintained females on food treatments that produced defined plastic and canalized periods, collected hemolymph every approximately 4 d, and determined the ages at which oviposition and the maximum Vg and TP titers occurred. Both Vg(max) titer and especially TP(max) titer were predictors of the number of eggs produced. The time from eclosion to Vg(max) was significantly affected by diet, but the time from Vg(max) to oviposition was not. Similarly, the time from eclosion to TP(max) was significantly affected by diet, while the time from TP(max) to oviposition was not. Hence, Vg(max) and TP(max) are physiological landmarks that occur during the canalized phase of egg production.     

An end to endless forms: epistasis, phenotype distribution bias, and nonuniform evolution

Studies of the evolution of development characterize the way in which gene regulatory dynamics during ontogeny constructs and channels phenotypic variation. These studies have identified a number of evolutionary regularities: (1) phenotypes occupy only a small subspace of possible phenotypes, (2) the influence of mutation is not uniform and is often canalized, and (3) a great deal of morphological variation evolved early in the history of multicellular life. An important implication of these studies is that diversity is largely the outcome of the evolution of gene regulation rather than the emergence of new, structural genes. Using a simple model that considers a generic property of developmental maps-the interaction between multiple genetic elements and the nonlinearity of gene interaction in shaping phenotypic traits-we are able to recover many of these empirical regularities. We show that visible phenotypes represent only a small fraction of possibilities. Epistasis ensures that phenotypes are highly clustered in morphospace and that the most frequent phenotypes are the most similar. We perform phylogenetic analyses on an evolving, developmental model and find that species become more alike through time, whereas higher-level grades have a tendency to diverge. Ancestral phenotypes, produced by early developmental programs with a low level of gene interaction, are found to span a significantly greater volume of the total phenotypic space than derived taxa. We suggest that early and late evolution have a different character that we classify into micro- and macroevolutionary configurations. These findings complement the view of development as a key component in the production of endless forms and highlight the crucial role of development in constraining biotic diversity and evolutionary trajectories.     

The ubiquity of phenotypic plasticity in plants: a synthesis

Adaptation to heterogeneous environments can occur via phenotypic plasticity, but how often this occurs is unknown. Reciprocal transplant studies provide a rich dataset to address this issue in plant populations because they allow for a determination of the prevalence of plastic versus canalized responses. From 31 reciprocal transplant studies, we quantified the frequency of five possible evolutionary patterns: (1) canalized response–no differentiation: no plasticity, the mean phenotypes of the populations are not different; (2) canalized response–population differentiation: no plasticity, the mean phenotypes of the populations are different; (3) perfect adaptive plasticity: plastic responses with similar reaction norms between populations; (4) adaptive plasticity: plastic responses with parallel, but not congruent reaction norms between populations; and (5) nonadaptive plasticity: plastic responses with differences in the slope of the reaction norms. The analysis included 362 records: 50.8% life‐history traits, 43.6% morphological traits, and 5.5% physiological traits. Across all traits, 52% of the trait records were not plastic, and either showed no difference in means across sites (17%) or differed among sites (83%). Among the 48% of trait records that showed some sort of plasticity, 49.4% showed perfect adaptive plasticity, 19.5% adaptive plasticity, and 31% nonadaptive plasticity. These results suggest that canalized responses are more common than adaptive plasticity as an evolutionary response to environmental heterogeneity.     

How to Explore Morphological Integration in Human Evolution and Development?

Most studies in evolutionary developmental biology focus on large-scale evolutionary processes using experimental or molecular approaches, whereas evolutionary quantitative genetics provides mathematical models of the influence of heritable phenotypic variation on the short-term response to natural selection. Studies of morphological integration typically are situated in-between these two styles of explanation. They are based on the consilience of observed phenotypic covariances with qualitative developmental, functional, or evolutionary models. Here we review different forms of integration along with multiple other sources of phenotypic covariances, such as geometric and spatial dependencies among measurements. We discuss one multivariate method [partial least squares analysis (PLS)] to model phenotypic covariances and demonstrate how it can be applied to study developmental integration using two empirical examples. In the first example we use PLS to study integration between the cranial base and the face in human postnatal development. Because the data are longitudinal, we can model both cross-sectional integration and integration of growth itself, i.e., how cross-sectional variance and covariance is actually generated in the course of ontogeny. We find one factor of developmental integration (connecting facial size and the length of the anterior cranial base) that is highly canalized during postnatal development, leading to decreasing cross-sectional variance and covariance. A second factor (overall cranial length to height ratio) is less canalized and leads to increasing (co)variance. In a second example, we examine the evolutionary significance of these patterns by comparing cranial integration in humans to that in chimpanzees.     

Plasticity of grasshopper vitellogenin production in response to diet is primarily a result of changes in fat body mass

Life history plasticity is the developmental production of different phenotypes by similar genotypes in response to different environments. Plasticity is common in early post-embryonic or adult development. Later in the developmental stage, the transition from developmentally plastic to canalized (i.e., inflexible) phases is often associated with the attainment of a threshold level of storage. Thresholds are often described simply as total body mass or cumulative consumption of food. The physiological characteristics of thresholds, such as the contributions of the growth of particular organs or the production rate of proteins, are largely unstudied. To address the physiology underlying a threshold-induced developmental transition, total vitellogenin production in response to diet quality in the lubber grasshopper was studied. For individuals that differed in age or dietary protein, somatic mass, ovarian mass, fat body mass, mass-specific vitellogenin production, vitellogenin titer, and storage protein titer were measured. Age and diet strongly affected these parameters, with ovarian mass and fat body mass contributing most to the differences. During mid vitellogenesis, females were highly plastic in response to changing food quality. Only during late vitellogenesis were females unresponsive to changes in food quality. Fat body mass was a more important component of plasticity than was mass-specific vitellogenin production. Because these two variables together make up total vitellogenin production, the greater contribution of fat body mass than mass-specific vitellogenin production suggests that growth factors may be more important than tissue stimulators in producing developmental changes in total vitellogenin production. To our knowledge, this is the first study to demonstrate that mass gain of an organ is more important to developmental plasticity than is the output of that same organ.     

Limb,tooth, beak: Three modes of development and evolutionary innovation of form

The standard model of evolutionary change of form, deriving from Darwin’s theory via the Modern Synthesis, assumes a gradualistic reshaping of anatomical structures, with major changes only occurring by many cycles of natural selection for marginal adaptive advantage. This model, with its assertion that a single mechanism underlies both micro- and macroevolutionary change, contains an implicit notion of development which is only applicable in some cases. Here we compare the embryological processes that shape the vertebrate limb bud, the mammalian tooth and the avian beak. The implied notion of development in the standard evolutionary picture is met only in the case of the vertebrate limb, a single-primordium organ with morphostatic shaping, in which cells rearrange in response to signalling centres which are essentially unchanged by cell movement. In the case of the tooth, a single-primordium organ with morphodynamic shaping in which the strengths and relationships between signalling centres is influenced by the cell and tissue movements they induce, and the beak, in which the final form is influenced by the collision and rearrangement of multiple tissue primordia, abrupt appearance of qualitatively different forms (i.e. morphological novelties) can occur with small changes in system parameters induced by a genetic change, or by an environmental factor whose effects can be subsequently canalized genetically. Bringing developmental mechanisms and, specifically, the material properties of tissues as excitable media into the evolutionary picture, demonstrates that gradualistic change for incremental adaptive advantage is only one of the possible modes of morphological evolution.     

Development in context: the timely emergence of eco-devo

Ecological development or 'eco-devo' examines the mechanisms of developmental regulation in real-world environments, providing an integrated approach for investigating both plastic and canalized aspects of phenotypic expression. This synthetic discipline brings a current understanding of environmentally mediated regulatory systems to studies of genetic variation, ecological function and evolutionary change. Eco-devo is emerging at a critical point in time, as researchers try to understand and predict the future of organisms in a changing world. Precise knowledge of the external and internal environmental cues, signaling pathways and genetic elements implicated in developmental outcomes will provide key insights to the immediate tolerance and potential evolutionary resilience of organisms to the altered physical and biotic conditions created by human activities.     

Developmental constraints on fin diversity

The fish fin is a breathtaking repository full of evolutionary diversity, novelty, and convergence. Over 500 million years, the adaptation to novel habitats has provided landscapes of fin diversity. Although comparative anatomy of evolutionarily divergent patterns over centuries has highlighted the fundamental architectures and evolutionary trends of fins, including convergent evolution, the developmental constraints on fin evolution, which bias the evolutionary trajectories of fin morphology, largely remain elusive. Here, we review the evolutionary history, developmental mechanisms, and evolutionary underpinnings of paired fins, illuminating possible developmental constraints on fin evolution. Our compilation of anatomical and genetic knowledge of fin development sheds light on the canalized and the unpredictable aspects of fin shape in evolution. Leveraged by an arsenal of genomic and genetic tools within the working arena of spectacular fin diversity, evolutionary developmental biology embarks on the establishment of conceptual framework for developmental constraints, previously enigmatic properties of evolution.     

Juvenile hormone is a marker of the onset of reproductive canalization in lubber grasshoppers

To meet the challenge of unpredictable environments, many animals are initially developmentally flexible (plastic) but then may become inflexible (canalized) at major developmental events. The control of reproductive output can undergo a switch from flexible to inflexible (Moehrlin, G.S., Juliano, S.A., 1998. Plasticity of insect reproduction: testing models of flexible and fixed development in response to different growth rates. Oecologia 115, 492-500), and juvenile hormone (JH) may control this switch. By manipulating food availability, we tested the hypothesis that JH is involved in the reproductive canalization that appears during oogenesis in lubber grasshoppers. We used four food treatments: (1) high (H); (2) high switched to low (HL); (3) low switched to high (LH); and (4) low (L). We collected hemolymph samples approximately every 4 days and measured the ages at which maximum JH level (JH(max)) and oviposition occurred. Diet significantly affected both age at JH(max) and age at oviposition. In contrast, diet had no significant effect on the time from JH(max) to oviposition nor on the maximum JH level observed. Our data demonstrate that, after JH(max) is reached, the time to oviposition in our grasshoppers was unresponsive to food availability. Hence, reproductive timing appears to be canalized after the JH(max). This is the first demonstration in a phytophagous insect that a particular factor (in this case, JH) can be used to mark the switch from reproductive plasticity to reproductive canalization.     

Hsp90 inhibition and the expression of phenotypic variability in the rainforest species Drosophila birchii

Recently a heat shock protein (Hsp90) has been implicated as controlling the expression of cryptic genetic variation through buffering developmental processes. The release of variability in canalized characters following Hsp90 inhibition has been established in model species including Drosophila melanogaster and Arabidopsis thaliana , but has not yet been examined in species with limited distributions. To test if Hsp90 has a role in releasing phenotypic variation in rainforest Drosophila species, developing larvae from a large (> 1000 individuals) outbred population of Drosophila birchii were treated with the Hsp90 inhibitors geldanamycin and radicicol, and morphological traits, desiccation resistance, and life-history traits were measured. The means of all traits were influenced by inhibition. Although only the phenotypic variances of two canalized bristle traits were affected consistently, variability for two of the continuously varying traits (fecundity and development time) were also affected, albeit inconsistently. There was also no effect of Hsp90 inhibition on the developmental stability of the morphological traits as measured by fluctuating asymmetry. Hsp90 inhibition did not increase phenotypic variability in desiccation resistance, a trait previously shown to represent an evolutionary limit in this species. These results question the extent to which Hsp90 buffers variation for both quantitative and discrete traits, and highlight the need for further empirical studies to determine the involvement of Hsp90 in canalization and developmental stability. Nevertheless the results demonstrated increased variability in canalized traits, consistent with observations in model systems. © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 457–465.     

Plasticity and canalization in the control of reproduction in the lubber grasshopper

The ability to change reproductive tactics during adult developmentin response to environmental variation is predicted to enhancefitness. Many organisms show phenotypic plasticity early innon-embryonic development, but later exhibit phases of developmentalinflexibility (=canalization). Therefore, we studied reproduction-relatedhormones and proteins and their relationships to plasticityin the Eastern lubber grasshopper. Diet-switching experimentsdemonstrated plasticity early in the egg production cycle, buta switch to canalization late in the cycle. We measured developmentaltiters of 4 hemolymph compounds from single individuals fromadult molt until first oviposition. These 4 compounds were theegg-yolk precursor protein vitellogenin, juvenile hormone (thecentral regulator of insect reproduction), major hemolymph proteins,and ecdysteroids (the arthropod molting hormone that ultimatelyis stored in the egg). Using diet manipulations, we investigatedhow these developmental titers relate to the switch from plasticto canalized egg production. All 4 hemolymph compounds reachedtheir peak levels during the canalized phase, about 12 day beforeoviposition. Diet switches after these peak levels did not affectthe timing to oviposition. Therefore, these peak titers werephysiological events that occurred after the individual committedto laying. We compared these patterns in reproduction to thedevelopment toward adult molt, another major life-history eventin insects. We observed an extended canalized phase before theadult molt. This canalized phase always included a peak of ecdysteroids.The similar patterns in the physiology of these life-historyevents suggested that common limitations may exist in majordevelopmental processes of insects that are directed by hormones.     

COSTS AND LIMITS OF PHENOTYPIC PLASTICITY IN ISLAND POPULATIONS OF THE COMMON FROG RANA TEMPORARIA UNDER DIVERGENT SELECTION PRESSURES

Costs and limits are assumed to be the major constraints on the evolution of phenotypic plasticity. However, despite their expected importance, they have been surprisingly hard to find in natural populations. It has therefore been argued that natural selection might have removed high-cost genotypes in all populations. However, if costs of plasticity are linked to the degree of plasticity expressed, then high costs of plasticity would only be present in populations where increased plasticity is under selection. We tested this hypothesis by investigating costs and limits of adaptive phenotypic plasticity in development time in a common garden study of island populations of the common frog Rana temporaria , which have varying levels of development time and phenotypic plasticity. Costs of plasticity were only found in populations with high-plastic genotypes, whereas the populations with the most canalized genotypes instead had a cost of canalization. Moreover, individuals displaying the most extreme phenotypes also were the most plastic ones, which mean we found no limits of plasticity. This suggests that costs of plasticity increase with increased level of plasticity in the populations, and therefore costs of plasticity might be more commonly found in high-plastic populations.     

Embryogenesis plasticity and the transmission of maternal effects in Daphnia pulex

Understanding how genetic, nongenetic, and environmental cues are integrated during development may be critical in understanding if, and how, organisms will respond to rapid environmental change. Normally, only post‐embryonic studies are possible. But in this study, we developed a real‐time, high‐throughput confocal microscope assay that allowed us to link Daphnia embryogenesis to offspring life history variation at the individual level. Our assay identified eight clear developmental phenotypes linked by seven developmental stages, the duration of which were correlated with the expression of specific offspring life history traits. Daphnia embryogenesis varied not only between clones reared in the same environment, but also within a single clone when mothers were of different ages or reared in different food environments. Our results support the hypothesis that Daphnia embryogenesis is plastic and can be altered by changes in maternal state or maternal environment. As well as furthering our understanding of the mechanisms underpinning parental effects, our assay may also have an industrial application if it can be used as a rapid ecotoxicological prescreen for testing the effect that pollutant doses have on offspring life histories traditionally assayed with a 21‐day Daphnia reproduction test.     

Do the antiherbivore traits of expanding leaves in the Neotropical tree Inga paraensis (Fabaceae) vary with light availability?

Treefall gaps in tropical forests have a profound effect on plants growing in the understory, primarily due to increased light availability. In higher light, mature leaves typically have increased anti-herbivore defenses. However, since the majority of herbivory occurs while leaves are expanding, it is important to determine whether defense expression during the short period of leaf expansion is canalized (invariant) or plastic in response to variation in light. Therefore, we examined young leaves of Inga paraensis (Fabaceae) saplings growing along a light gradient in a terra-firme forest in Central Amazonia. We quantified leaf production and expansion time, dry mass of phenolics, saponins, and nitrogen, ants attracted to extrafloral nectaries, and leaf consumption. Over the entire light gradient, the number of leaves produced per flush increased by 50?% and the mass of phenolic compounds by 20?%, but no other traits changed. On average, 39?% of leaf area was consumed with no difference across the light gradient. Alone, none of the leaf traits was a significant predictor of leaf consumption, except for phenolics, which showed a positive relationship. Multiple regressions showed that leaf consumption was positively related to more leaves per flush and a higher concentration of phenolics in leaves. Unlike studies of mature leaves, young leaves of I. paraensis show low plasticity in defense traits across a light gradient, suggesting that leaf development is canalized.     

Resource allocation during ontogeny is influenced by genetic,developmental and ecological factors in the horned beetle,Onthophagus taurus

Resource allocation trade-offs arise when developing organs are in competition for a limited pool of resources to sustain growth and differentiation. Such competition may constrain the maximal size to which structures can grow and may force a situation in which the evolutionary elaboration of one structure may only be possible at the expense of another. However, recent studies have called into question both the consistency and evolutionary importance of resource allocation trade-offs. This study focuses on a well-described trade-off between the horns and eyes of Onthophagus beetles and assesses the degree to which it is influenced by genetic, developmental and ecological conditions. Contrary to expectations, we observed that trade-off signatures (i) were mostly absent within natural populations, (ii) mostly failed to match naturally evolved divergences in horn investment among populations, (iii) were subject to differential changes in F₁ populations derived from divergent field populations and (iv) remained largely unaffected by developmental genetic manipulations of horn investment. Collectively, our results demonstrate that populations subject to different ecological conditions exhibit different patterns of, and differential plasticity in, resource allocation. Further, variation in ecological conditions, rather than canalized developmental mechanisms, may determine whether and to what degree morphological structures engage in resource allocation trade-offs.     

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.     

Synaptic competition in developmental binocular plasticity

A mathematical model of the possible physiological and biochemical mechanisms responsible for the changes occurring during binocular development is proposed. The model is based on the mechanisms postulated for the occurrence of well known plastic processes, such as posttetanic potentiation, sensitization and heterosynaptic inhibition. Because all these processes are of presynaptic nature, we have postulated that the plastic processes occurring during development are of the same nature. The factors we have considered in our model are: the transmitter pool size, the mobilization or synthesis of the transmitter, the transmitter release by the physiological stimulus, the neuroendocrine and genetic activity. With this model we have simulated the following phenomena during ocular development: (1) normal binocular development; (2) monocular deprivation, including the effects of reversing the occluded eye; (3) binocular deprivation and recovery; and (4) effects of alternating deprivation on mature binocularity. The model also allows us to explain in a natural way the possible changes occurring during denervation or disuse.     

How to become large quickly: quantitative genetics of growth and foraging in a flush feeding lepidopteran larva

Rapid larval growth in insects may be selected for by rapid ephemeral phenological changes in food resources modifying the structure of phenotypic and genetic (co)variation in and among individual traits. We studied the relative effects of three processes which can modify expression of additive genetic and nongenetic variation in traits. First, natural selection tends to erode genetic variation in fitness-related traits. Second, there may be high variance even in traits closely coupled with fitness, if these traits are themselves products of variable lower level traits. Third, traits may be canalized by developmental processes which reduce phenotypic variation. Moreover, we investigated the phenotypic and genetic role played by the underlying traits in attaining simultaneously both large size and short development time. We measured phenotypic and genetic (co)variation in several pre- and post-ingestive foraging traits, growth, development rate, development time and size, together forming a hierarchical network of traits, in the larvae of a flush feeding geometrid, Epirrita autumnata. Rapid larval growth rate and high pupal mass are closely related to fitness in E. autumnata. Traits closely associated with larval growth displayed low levels of additive genetic variation, indicating that genetic variability may have been exhausted by selection for rapid growth. The body size of E. autumnata, in spite of its close correlation with fitness, exhibited a significant additive genetic variation, possiblye because caterpillar size is the outcome of many underlying heritable traits. The low level traits in the hierarchical net, number (indicating larval movements) and size of feeding bouts in leaves, relative consumption rate and efficiency of conversion of ingested food, displayed high levels of residual variation. High residual variation in consumption and physiological ability to handle leaf material resulted from their flexibility which reduced variation in growth rate, i.e. growth rate was canalized. We did not detect a trade-off between development time and final size. On the contrary, large pupal masses were attained by short larval periods, and this relationship was strongly genetically determined, suggesting that both developmental time and final size are expressions of the same developmental process (vigorous growth) and the same genes (or linkage disequilibrium).     

Does local adaptation along a latitudinal cline shape plastic responses to combined thermal and nutritional stress?

Thermal and nutritional stress are commonly experienced by animals. This will become increasingly so with climate change. Whether populations can plastically respond to such changes will determine their survival. Plasticity can vary among populations depending on the extent of environmental heterogeneity. However, theory conflicts as to whether environmental heterogeneity should increase or decrease plasticity. Using three locally adapted populations of Drosophila melanogaster sampled from a latitudinal gradient, we investigated whether plastic responses to combinations of nutrition and temperature increase or decrease with latitude for four traits: egg-adult viability, egg-adult development time, and two body size traits. Employing nutritional geometry, we reared larvae on 25 diets varying in protein and carbohydrate content at two temperatures: 18 and 25°C. Plasticity varied among traits and across the three populations. Viability was highly canalized in all three populations. The tropical population showed the least plasticity for development time, the sub-tropical showed the highest plasticity for wing area, and the temperate population showed the highest plasticity for femur length. We found no evidence of latitudinal plasticity gradients in either direction. Our data highlight that differences in thermal variation and resource predictability experienced by populations along a latitudinal cline are not sufficient to predict their plasticity.