The Evolution of Modularity in the Mammalian Skull II: Evolutionary Consequences

Changes in patterns and magnitudes of integration may influence the ability of a species to respond to selection. Consequently, modularity has often been linked to the concept of evolvability, but their relationship has rarely been tested empirically. One possible explanation is the lack of analytical tools to compare patterns and magnitudes of integration among diverse groups that explicitly relate these aspects to the quantitative genetics framework. We apply such framework here using the multivariate response to selection equation to simulate the evolutionary behavior of several mammalian orders in terms of their flexibility, evolvability and constraints in the skull. We interpreted these simulation results in light of the integration patterns and magnitudes of the same mammalian groups, described in a companion paper. We found that larger magnitudes of integration were associated with a blur of the modules in the skull and to larger portions of the total variation explained by size variation, which in turn can exert a strong evolutionary constraint, thus decreasing the evolutionary flexibility. Conversely, lower overall magnitudes of integration were associated with distinct modules in the skull, to smaller fraction of the total variation associated with size and, consequently, to weaker constraints and more evolutionary flexibility. Flexibility and constraints are, therefore, two sides of the same coin and we found them to be quite variable among mammals. Neither the overall magnitude of morphological integration, the modularity itself, nor its consequences in terms of constraints and flexibility, were associated with absolute size of the organisms, but were strongly associated with the proportion of the total variation in skull morphology captured by size. Therefore, the history of the mammalian skull is marked by a trade-off between modularity and evolvability. Our data provide evidence that, despite the stasis in integration patterns, the plasticity in the magnitude of integration in the skull had important consequences in terms of evolutionary flexibility of the mammalian lineages.     

Animal learning as a source of developmental bias

As a form of adaptive plasticity that allows organisms to shift their phenotype toward the optimum, learning is inherently a source of developmental bias. Learning may be of particular significance to the evolutionary biology community because it allows animals to generate adaptively biased novel behavior tuned to the environment and, through social learning, to propagate behavioral traits to other individuals, also in an adaptively biased manner. We describe several types of developmental bias manifest in learning, including an adaptive bias, historical bias, origination bias, and transmission bias, stressing that these can influence evolutionary dynamics through generating nonrandom phenotypic variation and/or nonrandom environmental states. Theoretical models and empirical data have established that learning can impose direction on adaptive evolution, affect evolutionary rates (both speeding up and slowing down responses to selection under different conditions) and outcomes, influence the probability of populations reaching global optimum, and affect evolvability. Learning is characterized by highly specific, path‐dependent interactions with the (social and physical) environment, often resulting in new phenotypic outcomes. Consequently, learning regularly introduces novelty into phenotype space. These considerations imply that learning may commonly generate plasticity first evolution.     

Evolution,plasticity and evolving plasticity of phenology in the tree species Alnus glutinosa

Both traits and the plasticity of these traits are subject to evolutionary change and therefore affect the long‐term persistence of populations and their role in local communities. We subjected clones from 12 different populations of Alnus glutinosa, located along a latitudinal gradient, to two different temperature treatments, to disentangle the distribution of genetic variation in timing of bud burst and bud burst plasticity within and among genotypes, populations, and regions. We calculated heritability and evolvability estimates for bud burst and bud burst plasticity and assessed the influence of divergent selection relative to neutral drift. We observed higher levels of heritability and evolvability for bud burst than for its plasticity, whereas the total phenological heritability and evolvability (i.e. combining timing of bud burst and bud burst plasticity) suggest substantial evolutionary potential with respect to phenology. Earlier bud burst was observed for the low‐latitudinal populations than for the populations from higher latitudes, whereas the high‐latitudinal populations did not show the expected delayed bud burst. This countergradient variation can be due to evolution towards increased phenological plasticity at higher latitudes. However, because we found little evidence for adaptive differences in phenological plasticity across the latitudinal gradient, we suggest differential frost tolerance as the most likely explanation for the observed phenological patterns in A. glutinosa.     

THE EVOLVABILITY OF GROWTH FORM IN A CLONAL SEAWEED

Although modular construction is considered the key to adaptive growth or growth‐form plasticity in sessile taxa (e.g., plants, seaweeds and colonial invertebrates), the serial expression of genes in morphogenesis may compromise its evolutionary potential if growth forms emerge as integrated wholes from module iteration. To explore the evolvability of growth form in the red seaweed, Asparagopsis armata, we estimated genetic variances, covariances, and cross‐environment correlations for principal components of growth‐form variation in contrasting light environments. We compared variance–covariance matrices across environments to test environmental effects on heritable variation and examined the potential for evolutionary change in the direction of plastic responses to light. Our results suggest that growth form in Asparagopsis may constitute only a single genetic entity whose plasticity affords only limited evolutionary potential. We argue that morphological integration arising from modular construction may constrain the evolvability of growth form in Asparagopsis, emphasizing the critical distinction between genetic and morphological modularity in this and other modular taxa.     

Early developmental plasticity and integrative responses in arctic charr (Salvelinus alpinus): effects of water velocity on body size and shape

Environmental conditions such as temperature and water velocity may induce changes among alternative developmental pathways, i.e. phenotypic responses, in vertebrates. However, the extent to which the environment induces developmental plasticity and integrated developmental responses during early ontogeny of fishes remains poorly documented. We analyzed the responses of newly hatched Arctic charr (Salvelinus alpinus) to four experimental water velocities during 100 days of development. To our knowledge, this work is the first to analyze developmental plasticity responses of body morphology to an experimental gradient of water velocities during early ontogeny of fish. Arctic charr body size and shape responses show first, that morphometric traits display significant differences between low and high water velocities, thus revealing directional changes in body traits. Secondly, trait variation allows the recognition of critical ontogenetic periods that are most responsive to environmental constraints (40-70 and 80-90 days) and exhibit different levels of developmental plasticity. This is supported by the observation of asynchronous timing of variation peaks among treatments. Third, morphological interaction of traits is developmentally plastic and time-dependent. We suggest that developmental responses of traits plasticity and interaction at critical ontogenetic periods are congruent with specific environmental conditions to maintain the functional integrity of the organism.     

Multidimensional analysis of Drosophila wing variation in Evolution Canyon

Environmental stress has been suggested to be a major evolutionary force, both through inducing strong selection and because of its direct impact on developmental buffering processes that alter the evolvability of organisms. In particular, temperature has attracted much attention because of its importance as an ecological feature and the relative ease with which it can be experimentally manipulated in the lab. Evolution Canyon, Lower Nahal Oren, Israel, is a well studied natural site where ecological parameters are suspected to drive evolutionary differentiation. In this study, using Drosophila melanogaster isofemale lines derived from wild flies collected on both slopes of the canyon, we investigated the effect of developmental temperature upon the different components of phenotypic variation of a complex trait: the wing. Combining geometric and traditional morphometrics, we find only limited evidence for a differentiation among slopes. Investigating simultaneously phenotypic plasticity, genetic variation among isofemale lines, variation among individuals and fluctuating asymmetry, we could not identify a consistent effect of the stressful conditions encountered on the south facing slope. The prevailing structuring effect is that of the experimentally manipulated temperature which clearly influences wing mean size and shape. Variability, in contrast, is not consistently affected by temperature. Finally, we investigated the specific relationship between individual variation and fluctuating asymmetry. Using metric multi-dimensional scaling we show that the related patterns of wing shape variation are not identical, supporting the view that the underlying developmental processes are to a certain extent different.     

Developmental plasticity, morphological variation and evolvability: a multilevel analysis of morphometric integration in the shape of compound leaves

The structure of compound leaves provides flexibility for morphological change by variation in the shapes, sizes and arrangement of leaflets. Here, we conduct a multilevel analysis of shape variation in compound leaves to explore the developmental plasticity and evolutionary potential that are the basis of diversification in leaf shape. We use the methods of geometric morphometrics to study the shapes of individual leaflets and whole leaves in 20 taxa of Potentilla (sensu lato). A newly developed test based on the bootstrap approach suggests that uncertainty in the molecular phylogeny precludes firm conclusions whether there is a phylogenetic signal in the data on leaf shape. For variation among taxa, variation within taxa, as well as fluctuating asymmetry, there is evidence of strong morphological integration. The patterns of variation are similar across all three levels, suggesting that integration within taxa may act as a constraint on evolutionary change.     

Typology now: homology and developmental constraints explain evolvability

By linking the concepts of homology and morphological organization to evolvability, this paper attempts to (1) bridge the gap between developmental and phylogenetic approaches to homology and to (2) show that developmental constraints and natural selection are compatible and in fact complementary. I conceive of a homologue as a unit of morphological evolvability, i.e., as a part of an organism that can exhibit heritable phenotypic variation independently of the organism’s other homologues. An account of homology therefore consists in explaining how an organism’s developmental constitution results in different homologues/characters as units that can evolve independently of each other. The explanans of an account of homology is developmental, yet the very explanandum is an evolutionary phenomenon: evolvability in a character-by-character fashion, which manifests itself in phylogenetic patterns as recognized by phylogenetic approaches to homology. While developmental constraints and selection have often been viewed as antagonistic forces, I argue that both are complementary as they concern different parts of the evolutionary process. Developmental constraints, conceived of as the presence of the same set of homologues across phenotypic change, pertain to how heritable variation can be generated in the first place (evolvability), while natural selection operates subsequently on the produced variation.

Intraspecific variation in fruit size and shape in Corema album (Ericaceae) along a latitudinal gradient: from fruits to populations

Plant trait variation can be the result of environmental variability, developmental instability, and plasticity, although it can also arise from previous selective pressures on fruit traits themselves or directly on their variation. We aimed to quantify fruit size and shape variability at within‐plant, among‐plant, among‐population, and among‐year levels. For 2 years, we measured fruit size and shape along the geographical range of Corema album, aiming to determine whether (1) the population level among‐plant variation is lower than within‐plant and among‐population variation and (2) the ratio of within‐plant to among‐plant variation follows a latitudinal pattern. Levels of fruit variation were in accordance with the reported mean levels for reproductive organs. Most variance concentrated on within‐ and among‐individual levels for size, showing higher values for among‐individual variation in fruit shape. Although fruit size retained important variation among populations, this source of variance was negligible for fruit shape. This difference could arise from contrasting mechanical or developmental constraints. Despite the marked climatic differences along the latitudinal range of the species, latitude did not affect the ratio of within‐ to among‐plant variation. We show that an analysis of the often‐disregarded sources of intraspecific variation can produce unexpected results that deserve further investigation.     

Genome size and developmental complexity

Haploid genome size (C-value) is correlated positively with cell size, and negatively with cell division rate, in a variety of taxa. Because these associations are causative, genome size has the potential to impact (and in turn, be influenced by) organism-level characters affected by variation in either of these cell-level parameters. One such organismal feature is development. Developmental rate, in particular, has been associated with genome size in numerous plant, vertebrate, and invertebrate groups. However, rate is only one side of the developmental coin; the other important component is complexity. When developmental complexity is held essentially constant, as among many plants, developmental rate is the visibly relevant parameter. In this case, genome size can impose thresholds on developmental lifestyle (and vice versa), as among annual versus perennial plants. When developmental rate is constrained (as during time-limited amphibian metamorphosis), complexity becomes the notable variable. An appreciation for this rate-complexity interaction has so far been lacking, but is essential for an understanding of the relationships between genome size and development. Moreover, such an expanded view may help to explain patterns of variation in taxa as diverse as insects and fish. In each case, a hierarchical approach is necessary which recognizes the complex interaction of evolutionary processes operating at several levels of biological organization.     

Historical and philosophical perspectives on the study of developmental bias

Throughout the recent history of research at the intersection of evolution and development, notions such as developmental constraint, evolutionary novelty, and evolvability have been prominent, but the term “developmental bias” has scarcely been used. And one may even doubt whether a unique and principled definition of bias is possible. I argue that the concept of developmental bias can still play a vital scientific role by means of setting an explanatory agenda that motivates investigation and guides the formulation of integrative explanatory frameworks. Less crucial is a definition that would classify patterns of phenotypic variation and unify variational patterns involving different traits and taxa as all being “bias.” Instead, what we should want is a concept that generates intellectual identity across various researchers, and that unites the diverse fields and approaches relevant to the study of developmental bias, from paleontology to behavioral biology. I point to some advantages of conducting research specifically under the label of “developmental bias,” compared with employing other, more common terms such as “evolvability.”     

Allometric and nonallometric components of Drosophila wing shape respond differently to developmental temperature

Phenotypic plasticity of wing size and shape of Drosophila simulans was analyzed across the entire range of viable developmental temperatures with Procrustes geometric morphometric method. In agreement with previous studies, size clearly decreases when temperature increases. Wing shape variation was decomposed into its allometric (24%) and nonallometric (76%) components, and both were shown to involve landmarks located throughout the entire wing blade. The allometric component basically revealed a progressive, monotonous variation along the temperature. Surprisingly, nonallometric shape changes were highly similar at both extremes of the thermal range, suggesting that stress, rather than temperature per se, is the key developmental factor affecting wing shape.     

Developmental responses to early‐life adversity: Evolutionary and mechanistic perspectives

Adverse ecological and social conditions during early life are known to influence development, with rippling effects that may explain variation in adult health and fitness. The adaptive function of such developmental plasticity, however, remains relatively untested in long‐lived animals, resulting in much debate over which evolutionary models are most applicable. Furthermore, despite the promise of clinical interventions that might alleviate the health consequences of early‐life adversity, research on the proximate mechanisms governing phenotypic responses to adversity have been largely limited to studies on glucocorticoids. Here, we synthesize the current state of research on developmental plasticity, discussing both ultimate and proximate mechanisms. First, we evaluate the utility of adaptive models proposed to explain developmental responses to early‐life adversity, particularly for long‐lived mammals such as humans. In doing so, we highlight how parent‐offspring conflict complicates our understanding of whether mothers or offspring benefit from these responses. Second, we discuss the role of glucocorticoids and a second physiological system—the gut microbiome—that has emerged as an additional, clinically relevant mechanism by which early‐life adversity can influence development. Finally, we suggest ways in which nonhuman primates can serve as models to study the effects of early‐life adversity, both from evolutionary and clinical perspectives.     

Evolutionary reduction of developmental plasticity in desert spadefoot toads

Organisms vary their rates of growth and development in response to environmental inputs. Such developmental plasticity may be adaptive and positively correlate with environmental heterogeneity. However, the evolution of developmental plasticity among closely related taxa is not well understood. To determine the evolutionary pattern of plasticity, we compared plasticity in time to and size at metamorphosis in response to water desiccation in tadpoles among spadefoot species that differ in breeding pond and larval period durations. Like most tadpoles, spadefoot tadpoles possess the remarkable ability to accelerate development in response to pond drying to avoid desiccation. Here, we hypothesize that desert spadefoot tadpoles have evolved reduced plasticity to avoid desiccation in ephemeral desert pools compared to their nondesert relatives that breed in long-duration ponds. We recorded time to and size at metamorphosis following experimental manipulation of water levels and found that desert-adapted species had much less plasticity in larval period and size at metamorphosis than nondesert species, which retain the hypothetical ancestral state of plasticity. Furthermore, we observed a correlation between degree of plasticity and fat body content that may provide mechanistic insights into the evolution of developmental plasticity in amphibians.     

Deciphering the Palimpsest: Studying the Relationship Between Morphological Integration and Phenotypic Covariation

Organisms represent a complex arrangement of anatomical structures and individuated parts that must maintain functional associations through development. This integration of variation between functionally related body parts and the modular organization of development are fundamental determinants of their evolvability. This is because integration results in the expression of coordinated variation that can create preferred directions for evolutionary change, while modularity enables variation in a group of traits or regions to accumulate without deleterious effects on other aspects of the organism. Using our own work on both model systems (e.g., lab mice, avians) and natural populations of rodents and primates, we explore in this paper the relationship between patterns of phenotypic covariation and the developmental determinants of integration that those patterns are assumed to reflect. We show that integration cannot be reliably studied through phenotypic covariance patterns alone and argue that the relationship between phenotypic covariation and integration is obscured in two ways. One is the superimposition of multiple determinants of covariance in complex systems and the other is the dependence of covariation structure on variances in covariance-generating processes. As a consequence, we argue that the direct study of the developmental determinants of integration in model systems is necessary to fully interpret patterns of covariation in natural populations, to link covariation patterns to the processes that generate them, and to understand their significance for evolutionary explanation.     

Adaptive maternal behavioral plasticity and developmental programming mitigate the transgenerational effects of temperature in dung beetles

Phenotypic plasticity allows organisms to cope with rapid environmental change. Yet exactly when during ontogeny plastic responses are elicited, whether plastic responses produced in one generation influence phenotypic variation and fitness in subsequent generations, and the role of plasticity in shaping population divergences, remains overall poorly understood. Here, we use the dung beetle Onthophagus taurus to assess plastic responses to temperature at several life stages bridging three generations and compare these responses across three recently diverged populations. We find that beetles reared at hotter temperatures grow less than those reared at mild temperatures, and that this attenuated growth has transgenerational consequences by reducing offspring size and survival in subsequent generations. However, we also find evidence that plasticity may mitigate these consequences in two ways: 1) mothers modify the temperature of their offspring's developmental environment via behavioral plasticity and 2) in one population, offspring exhibit accelerated growth when exposed to hot temperatures during very early development (‘developmental programming’). Lastly, our study reveals that offspring responses to temperature diverged among populations in fewer than 100 generations, possibly in response to range‐specific changes in climatic or social conditions.     

A developmental morphologist's perspective on plasticity

This series of essays addresses plasticity from the perspective of developmental morphology. The first essay deals with the problem of distinguishing between plasticity and other types of ontogenetic variation. In a temporally varying environment, morphological plasticity may be expressed as the production of a succession of different metamers. However, even in a constant environment, plant metamers can vary dramatically, a phenomenon known as heteroblasty. Because heteroblasty and plasticity can yield similar patterns of ontogenetic variation, the two are often confounded in analyses of developmental plasticity. The second essay discusses the integration of plant phenotypic responses and finds that the evidence for integration is equivocal. The third section shows that developmental properties can constrain the expression of morphological plasticity. Developmental lags and the epiphenotype problem are particularly important features for analyses of the evolution and expression of plasticity. Finally, in answer to the question of strategies for studying plasticity, I emphasize the need for research at multiple levels and for the inclusion of a historical or phylogenetic perspective.     

Evolvability as the proper focus of evolutionary developmental biology

SUMMARY Research conducted under the label of evolutionary developmental biology has tended to revolve around a few central issues such as modularity, integration, and canalization. Yet, as the field has grown, it has become increasingly difficult to define in terms of its central question and relation to broader evolutionary concerns. We argue that these central issues of evo-devo gain their currency from connections to a central question that defines the field, and we propose that this central question is about the nature of evolvability. However, not all research currently carried out under the label of "evo-devo" speaks to this focal concern. The aim of this article is therefore to argue for a precise formulation of evolutionary developmental biology's core question.     

Effects of parental radiation exposure on developmental instability in grasshoppers

Mutagenic and epigenetic effects of environmental stressors and their transgenerational consequences are of interest to evolutionary biologists because they can amplify natural genetic variation. We studied the effect of parental exposure to radioactive contamination on offspring development in lesser marsh grasshopper Chorthippus albomarginatus. We used a geometric morphometric approach to measure fluctuating asymmetry (FA), wing shape and wing size. We measured time to sexual maturity to check whether parental exposure to radiation influenced offspring developmental trajectory and tested effects of radiation on hatching success and parental fecundity. Wings were larger in early maturing individuals born to parents from high radiation sites compared to early maturing individuals from low radiation sites. As time to sexual maturity increased, wing size decreased but more sharply in individuals from high radiation sites. Radiation exposure did not significantly affect FA or shape in wings nor did it significantly affect hatching success and fecundity. Overall, parental radiation exposure can adversely affect offspring development and fitness depending on developmental trajectories although the cause of this effect remains unclear. We suggest more direct measures of fitness and the inclusion of replication in future studies to help further our understanding of the relationship between developmental instability, fitness and environmental stress.