以发育模块重复征用和整合为基础的进化创新机制

进化新征的起源和分化是进化发育生物学研究的核心问题。通过对多细胞生物早期发育调控机制的比较分析,发现亲缘关系较远的生物所共有的一些形态特征受保守的发育调控程序调节（深同源性）。许多创新性状的发生是基于对预先存在的基因或发育调控模块的重复利用和整合。发育基因调控网络在结构和功能上高度模块化,因此不仅可以通过模块拆分和重复征用改变发育程式,而且也增强了调控网络自身的进化力。研究基因调控网络和发育系统的进化动态将有助于更深入地认识生物演化过程中创新性状发生和表型进化的分子机制。     

Fossil evidence for key innovations in the evolution of insect diversity

Explaining the taxonomic richness of the insects, comprising over half of all described species, is a major challenge in evolutionary biology. Previously, several evolutionary novelties (key innovations) have been posited to contribute to that richness, including the insect bauplan, wings, wing folding and complete metamorphosis, but evidence over their relative importance and modes of action is sparse and equivocal. Here, a new dataset on the first and last occurrences of fossil hexapod (insects and close relatives) families is used to show that basal families of winged insects (Palaeoptera, e.g. dragonflies) show higher origination and extinction rates in the fossil record than basal wingless groups (Apterygota, e.g. silverfish). Origination and extinction rates were maintained at levels similar to Palaeoptera in the more derived Polyneoptera (e.g. cockroaches) and Paraneoptera (e.g. true bugs), but extinction rates subsequently reduced in the very rich group of insects with complete metamorphosis (Holometabola, e.g. beetles). Holometabola show evidence of a recent slow-down in their high net diversification rate, whereas other winged taxa continue to diversify at constant but low rates. These data suggest that wings and complete metamorphosis have had the most effect on family-level insect macroevolution, and point to specific mechanisms by which they have influenced insect diversity through time.     

Evolution of networks for body plan patterning; interplay of modularity, robustness and evolvability

A major goal of evolutionary developmental biology (evo-devo) is to understand how multicellular body plans of increasing complexity have evolved, and how the corresponding developmental programs are genetically encoded. It has been repeatedly argued that key to the evolution of increased body plan complexity is the modularity of the underlying developmental gene regulatory networks (GRNs). This modularity is considered essential for network robustness and evolvability. In our opinion, these ideas, appealing as they may sound, have not been sufficiently tested. Here we use computer simulations to study the evolution of GRNs' underlying body plan patterning. We select for body plan segmentation and differentiation, as these are considered to be major innovations in metazoan evolution. To allow modular networks to evolve, we independently select for segmentation and differentiation. We study both the occurrence and relation of robustness, evolvability and modularity of evolved networks. Interestingly, we observed two distinct evolutionary strategies to evolve a segmented, differentiated body plan. In the first strategy, first segments and then differentiation domains evolve (SF strategy). In the second scenario segments and domains evolve simultaneously (SS strategy). We demonstrate that under indirect selection for robustness the SF strategy becomes dominant. In addition, as a byproduct of this larger robustness, the SF strategy is also more evolvable. Finally, using a combined functional and architectural approach, we determine network modularity. We find that while SS networks generate segments and domains in an integrated manner, SF networks use largely independent modules to produce segments and domains. Surprisingly, we find that widely used, purely architectural methods for determining network modularity completely fail to establish this higher modularity of SF networks. Finally, we observe that, as a free side effect of evolving segmentation and differentiation in combination, we obtained in-silico developmental mechanisms resembling mechanisms used in vertebrate development.     

The evolutionary origins of modularity

A central biological question is how natural organisms are so evolvable (capable of quickly adapting to new environments). A key driver of evolvability is the widespread modularity of biological networks—their organization as functional, sparsely connected subunits—but there is no consensus regarding why modularity itself evolved. Although most hypotheses assume indirect selection for evolvability, here we demonstrate that the ubiquitous, direct selection pressure to reduce the cost of connections between network nodes causes the emergence of modular networks. Computational evolution experiments with selection pressures to maximize network performance and minimize connection costs yield networks that are significantly more modular and more evolvable than control experiments that only select for performance. These results will catalyse research in numerous disciplines, such as neuroscience and genetics, and enhance our ability to harness evolution for engineering purposes.     

Evolvability of the Primate Pelvic Girdle

The ilium and ischiopubic bones of the pelvis arise from different regulatory pathways, and as a result, they may be modular in their organization such that features on one bone may be morphologically integrated with each other, but not with features on the other pelvic bone. Modularity at this gross level of organization can act to increase the ability of these structures to respond to selection pressures (i.e., their evolvability). Furthermore, recent work has suggested that the evolution of the human pelvis was facilitated by low levels of integration and high levels of evolvability relative to other African apes. However, the extent of morphological integration and modularity of the bones of the pelvic girdle is not well understood, especially across the entire order of primates. Therefore, the hypothesis that the ilium and ischiopubis constitute separate modules was tested using three-dimensional landmark data that were collected from 752 pelves from 35 primate species. In addition, the hypothesis that the human pelvis demonstrates greatest evolvability was tested by comparing it to all other primates. The results demonstrate that regardless of phylogeny and locomotor function, the primate pelvis as a whole is characterized by low levels of overall integration and high levels of evolvability. In addition, the results support the developmental hypothesis of separate ilium and ischiopubis modular units. Finally, all primates, including humans, apparently share a common pattern of integration, modularity, and evolvability in the pelvis.     

Uracil-containing DNA in Drosophila: stability, stage-specific accumulation, and developmental involvement

Base-excision repair and control of nucleotide pools safe-guard against permanent uracil accumulation in DNA relying on two key enzymes: uracil-DNA glycosylase and dUTPase. Lack of the major uracil-DNA glycosylase UNG gene from the fruit fly genome and dUTPase from fruit fly larvae prompted the hypotheses that i) uracil may accumulate in Drosophila genomic DNA where it may be well tolerated, and ii) this accumulation may affect development. Here we show that i) Drosophila melanogaster tolerates high levels of uracil in DNA; ii) such DNA is correctly interpreted in cell culture and embryo; and iii) under physiological spatio-temporal control, DNA from fruit fly larvae, pupae, and imago contain greatly elevated levels of uracil (200-2,000 uracil/million bases, quantified using a novel real-time PCR-based assay). Uracil is accumulated in genomic DNA of larval tissues during larval development, whereas DNA from imaginal tissues contains much less uracil. Upon pupation and metamorphosis, uracil content in DNA is significantly decreased. We propose that the observed developmental pattern of uracil-DNA is due to the lack of the key repair enzyme UNG from the Drosophila genome together with down-regulation of dUTPase in larval tissues. In agreement, we show that dUTPase silencing increases the uracil content in DNA of imaginal tissues and induces strong lethality at the early pupal stages, indicating that tolerance of highly uracil-substituted DNA is also stage-specific. Silencing of dUTPase perturbs the physiological pattern of uracil-DNA accumulation in Drosophila and leads to a strongly lethal phenotype in early pupal stages. These findings suggest a novel role of uracil-containing DNA in Drosophila development and metamorphosis and present a novel example for developmental effects of dUTPase silencing in multicellular eukaryotes. Importantly, we also show lack of the UNG gene in all available genomes of other Holometabola insects, indicating a potentially general tolerance and developmental role of uracil-DNA in this evolutionary clade.     

Metamorphic remodeling of a planktotrophic larva to produce the predatory feeding system of a cone snail (Mollusca, Neogastropoda)

I used histological sections and 3D reconstructions to document development through metamorphosis of the foregut and proboscis in the conoidean neogastropod Conus lividus. A goal was to determine how highly derived features of the post-metamorphic feeding system of this gastropod predator develop without interfering with larval structures for microherbivory. A second goal was to compare foregut development in this conoidean with previous observations on foregut development in the buccinoidean neogastropod Nassarius mendicus. These two neogastropods both have a feeding larval stage, but they show major differences in post-metamorphic foregut morphology. Basic events in development of the proboscis and proboscis sheath in C. lividus and N. mendicus were similar. However, the elongate buccal tube of C. lividus forms during metamorphosis as a composite of apical epidermal tissue that grows inward and ventral foregut tissue that extends outward. The larval mouth is not carried through metamorphosis. Comparative observations on foregut development in caenogastropods, which now include data on C. lividus, suggest that the foregut incorporates dorsal and ventral modules having different ontogenetic and functional fates. This developmental modularity may have facilitated evolutionary diversification of the post-metamorphic foregut. Foregut diversification in predatory gastropods may have been further fast-tracked by developmental uncoupling of larval and post-metamorphic mouths.     

On the origin of modular variation

We study the dynamics of modularization in a minimal substrate. A module is a functional unit relatively separable from its surrounding structure. Although it is known that modularity is useful both for robustness and for evolvability (Wagner 1996), there is no quantitative model describing how such modularity might originally emerge. Here we suggest, using simple computer simulations, that modularity arises spontaneously in evolutionary systems in response to variation, and that the amount of modular separation is logarithmically proportional to the rate of variation. Consequently, we predict that modular architectures would appear in correlation with high environmental change rates. Because this quantitative model does not require any special substrate to occur, it may also shed light on the origin of modular variation in nature. This observed relationship also indicates that modular design is a generic phenomenon that might be applicable to other fields, such as engineering: Engineering design methods based on evolutionary simulation would benefit from evolving to variable, rather than stationary, fitness criteria, as a weak and problem-independent method for inducing modularity.     

The Developmental Basis of Variational Modularity: Insights from Quantitative Genetics,Morphometrics, and Developmental Biology

Groups of correlated characters (variational modules) often are considered to be the result of dissociated local developmental factors, i.e., of a modular genotype–phenotype map. But certain sets of pleiotropic factors can equally well induce modular phenotypic variation—no local developmental factors are necessary for a modular covariance structure. It is thus not possible to infer genetic or developmental modularity from standing variation alone. Yet, only for approximately linear genotype–phenotype maps is the induced covariance structure stable over changes of the phenotypic mean. For larger genetic and phenotypic variation, such as on a macroevolutionary level, developmental effects often are nonlinear and variational modularity remains stable only when it is realized by local dissociated developmental factors with no overlap of pleiotropic ranges. The evo-devo concept of modularity concurs only at this macroevolutionary level with the quantitative notion of variational modularity. Empirical evidence on the genetic and developmental architecture underlying phenotypic variation is inconclusive and partly subject to methodological problems. Many studies seem to indicate modularized phenotypic variation and local clusters of QTL effects, whereas other studies find support for several alternative models of modularity and report continuous distributions of QTL effects. This inconsistency partly results from the neglect of spatial relationships among the measured traits. Given the complex development of higher organisms, a combination of pleiotropic factors and more local developmental effects with a hierarchical, overlapping, and more or less continuous distribution appears most likely.     

Shifts in hexapod diversification and what Haldane could have said

Data on species richness and taxon age are assembled for the extant hexapod orders (insects and their six-legged relatives). Coupled with estimates of phylogenetic relatedness, and simple statistical null models, these data are used to locate where, on the hexapod tree, significant changes in the rate of cladogenesis (speciation-minus-extinction rate) have occurred. Significant differences are found between many successive pairs of sister taxa near the base of the hexapod tree, all of which are attributable to a shift in diversification rate after the origin of the Neoptera (insects with wing flexion) and before the origin of the Holometabola (insects with complete metamorphosis). No other shifts are identifiable amongst supraordinal taxa. Whilst the Coleoptera have probably diversified faster than either of their putative sister lineages, they do not stand out relative to other closely related clades. These results suggest that any Creator had a fondness for a much more inclusive clade than the Coleoptera, definitely as large as the Eumetabola (Holometabola plus bugs and their relatives), and possibly as large as the entire Neoptera. Simultaneous, hence probable causative events are discussed, of which the origin of wing flexion has been the focus of much attention.     

DISSECTION OF EVOLUTIONARY NETWORKS TO ASSESS THEIR ROLE IN THE EVOLUTION OF ROBUSTNESS,FUNCTION, AND DIVERSIFICATION

Biological systems are remarkably robust in the face of environmental, mutational, and developmental perturbations. Analyses of molecular networks reveal recurrent features, such as modularity, that have been implicated in robustness and evolvability. Multiple theoretical models account for these features, yet few empirical tests of these models exist. Here I develop a set of broadly applicable methodologies to enable expanded empirical evaluation of model predictions. The methodologies focus on the inference and analysis of networks that depict evolutionary correlations among characters. I apply these methodologies to analyze an evolutionary network at a larger scale of organization among 42 stem anatomical and morphological characters of 52 species in the genus Adenia (Passifloraceae). I evaluate a model predicting that modular evolutionary networks will evolve in response to environmental change. The evolutionary network of Adenia is modular and “small‐world,” and the three diagnosed modules correspond roughly to functions of transport, storage, and mechanical support. The phylogenetically informed analyses suggest that the storage module is more impacted by environmental change than expected by chance. These results corroborate the hypothesis that modularity reduces the impact of environmental change, but this result requires further empirical evaluation that can be aided by the proposed methods in additional study systems.     

The modular organization of roe deer (<Emphasis Type="Italic">Capreolus capreolus</Emphasis>) body during ontogeny: the effects of sex and habitat

Background

As a small artiodactyl, the roe deer (Capreolus capreolus L.) is characterized by biological plasticity and great adaptability demonstrated by their survival under a wide variety of environmental conditions. In order to depict patterns of phenotypic variation of roe deer body this study aims to quantify variation during ontogenetic development and determine how sex-specific reproductive investment and non-uniform habitat differences relate to phenotypic variation and do these differential investments mold the patterns of phenotypic variation through modular organisation.

Results

Patterns of phenotypic correlation among body traits change during the ontogeny of roe deer, with differential influence of sex and habitat type. Modularity was found to be a feature of closed habitats with trunk+forelimbs+hindlimbs as the best supported integration/modularity hypothesis for both sexes. The indices of integration and evolvability vary with habitat type, age and sex where increased integration is followed by decreased evolvability.

Conclusion

This is the first study that quantifies patterns of correlation in the roe deer body and finds pronounced changes in correlation structure during ontogeny affected by sex and habitat type. The correlation structure of the roe deer body is developmentally written over the course of ontogeny but we do not exclude the influence of function on ontogenetic changes. Modularity arises with the onset of reproduction (subadults not being modular) and is differentially expressed in males and females from different habitats. Both adult males and females show modularity in primordial, closed habitats. Overall, all these findings are important as they provide support to the idea that modularity can evolve at the population level and change fast within a species.

     

Phenoptosis in arthropods and immortality of social insects

In general, there are no drastic differences in phenoptosis patterns in plant and animal organisms. However, there are some specific features characteristic for insects and other arthropods: 1) their development includes metamorphosis with different biochemical laws at consecutive developmental stages; 2) arthropods can reduce or stop development and aging when in a state of diapause or temporal cold immobility; 3) their life cycle often correlates with seasonal changes of surroundings; 4) polymorphism is widespread — conspecifics differ by their lifespans and phenoptosis features; 5) lifespan-related sexual dimorphism is common; 6) significant situational plasticity of life cycle organization is an important feature; for example, the German wasp (Paravespula germanica) is obligatorily univoltine in the temperate zone, while in tropical regions its lifespan increases and leads to repeated reproduction; 7) life cycles of closely related species may differ significantly, for example, in contrast to German wasp, some tropical hornets (Vespa) have only one reproduction period. Surprisingly, many insect species have been shown to be subjected to gradual aging and phenoptosis, like the highest mammals. However, queens of social insects and some long-lived arachnids can apparently be considered non-aging organisms. In some species, lifespan is limited to one season, while others live much longer or shorter. Cases of one-time reproduction are rather rare. Aphagia is common in insects (over 10,000 species). Cannibalism is an important mortality factor in insects as well as in spiders. In social insects, which exist only in colonies (families), the lifetime of a colony can be virtually unlimited. However, in case of some species the developmental cycle and death of a colony after its completion are predetermined. Most likely, natural selection in insects does not lengthen individual lifespan, but favors increase in reproduction efficiency based on fast succession of generations leading to increased evolvability.     

Conserved developmental processes and the formation of evolutionary novelties: examples from butterfly wings

The origin and diversification of evolutionary novelties-lineage-specific traits of new adaptive value-is one of the key issues in evolutionary developmental biology. However, comparative analysis of the genetic and developmental bases of such traits can be difficult when they have no obvious homologue in model organisms. The finding that the evolution of morphological novelties often involves the recruitment of pre-existing genes and/or gene networks offers the potential to overcome this challenge. Knowledge about shared developmental processes obtained from extensive studies in model organisms can then be used to understand the origin and diversification of lineage-specific structures. Here, we illustrate this approach in relation to eyespots on the wings of Bicyclus anynana butterflies. A number of spontaneous mutations isolated in the laboratory affect eyespots, lepidopteran-specific features, and also processes that are shared by most insects. We discuss how eyespot mutants with disturbed embryonic development may help elucidate the genetic pathways involved in eyespot formation, and how venation mutants with altered eyespot patterns might shed light on mechanisms of eyespot development.     

Modularity in the evolution of yeast protein interaction network

Protein interaction networks are known to exhibit remarkable structures: scale-free and small-world and modular structures. To explain the evolutionary processes of protein interaction networks possessing scale-free and small-world structures, preferential attachment and duplication-divergence models have been proposed as mathematical models. Protein interaction networks are also known to exhibit another remarkable structural characteristic, modular structure. How the protein interaction networks became to exhibit modularity in their evolution? Here, we propose a hypothesis of modularity in the evolution of yeast protein interaction network based on molecular evolutionary evidence. We assigned yeast proteins into six evolutionary ages by constructing a phylogenetic profile. We found that all the almost half of hub proteins are evolutionarily new. Examining the evolutionary processes of protein complexes, functional modules and topological modules, we also found that member proteins of these modules tend to appear in one or two evolutionary ages. Moreover, proteins in protein complexes and topological modules show significantly low evolutionary rates than those not in these modules. Our results suggest a hypothesis of modularity in the evolution of yeast protein interaction network as systems evolution.     

Developmental plasticity associated with early structural integration and evolutionary patterns: Examples of developmental bias and developmental facilitation in the skeletal system

The relation of developmental plasticity to evolutionary diversification is a key component of evolutionary theory involving developmental bias, but the basis of the relationship varies among traits and among taxa. Here I review some scenarios of how structural integration during early organogenesis could influence this relationship. When condensations are highly integrated and dependent on each other during early organogenesis, both plasticity and evolution are restricted, for example size proportions in molar tooth rows and phalanges within a digit. When similar condensations develop and remain separate (in tracheal cartilages and feather buds), they show high levels of variation and diversity in number but not in shape and size, at least at early stages. When non‐similar structures form separately and then integrate while still undergoing patterning, high levels of plasticity (in number, size, shape; in rib uncinate processes) or new dimensions of ecologically‐significant variation (cusp offset, in mammal teeth) are seen. Although each of these structural integration scenarios is unique, the modulation of evolvability is detectable and informative. Parsing the influence of structural integration at these developmental levels, rather than later‐stage structural correlations or only through genetic covariation, may be necessary to advance understanding of evolvability of the phenotype.     

What are and what are not imaginal discs: reevaluation of some basic concepts (Insecta, Holometabola).

Some general aspects of the concept of imaginal discs in the Holometabola are reevaluated. Their monolayer character and continuity with the surrounding epidermis are confirmed. Studies on the imaginal discs of the silkworm (Bombyx mori) and data from the literature show that the discs and their peripodial cells produce cuticle during larval life, as well as at metamorphosis. In B. mori it is demonstrated that adult and larval antennae are produced by the same cells or their progeny. The results also suggest that segments of the typically three-segmented larval antenna of Holometabola are not scape, pedicel, and one-segmented flagellum; at least segments 2 and 3 are of flagellar origin. Based on these and some additional facts it is argued that: (1) No larval organs are "replaced" at metamorphosis, but strict "sequential homology" is always maintained. (2) Imaginal discs are not undifferentiated structures destined to form the adult after larval breakdown, cannot be unambiguously defined, and do not represent qualitatively different epidermal structures. Classical imaginal discs (invaginated and present also in pre-final larval instars) arose several times independently and were not present in the larvae of ancestral Holometabola. (3) Since the disc cells are not undifferentiated and "embryonic" (if these words have a defined meaning at all), it is unreasonable to expect that the processes taking place in discs at metamorphosis would differ fundamentally from those occurring in other diploid metamorphosing epidermal cells.     

What is an individual organism? A multilevel selection perspective

Most biologists implicitly define an individual organism as "one genome in one body." This definition is based on physiological and genetic criteria, but it is problematic for colonial organisms. We propose a definition based instead on the evolutionary criteria of alignment of fitness, export of fitness by germ-soma specialization, and adaptive functional organization. We consider how these concepts apply to various putative individual organisms. We conclude that complex multicellular organisms and colonies of eusocial insects satisfy these three criteria, but that, in most cases (with at least one notable exception), colonies of modular organisms and genetic chimeras do not. While species do not meet these criteria, they may meet the criteria for a broader concept--that of an evolutionary individual--and sexual reproduction may be a species-level exaptation for enhancing evolvability. We also review the costs and benefits of internal genetic heterogeneity within putative individuals, demonstrating that high relatedness is neither a necessary nor a sufficient condition for individuality, and that, in some cases, genetic variability may have adaptive benefits at the level of the whole.     

Fitness consequences of the timing of metamorphosis in a freshwater crustacean

Metamorphosis is a common life-cycle transition in organisms as diverse as amphibians, insects, fishes and crustaceans, and the timing of this transition often affects an individual's fitness. Here, we measured age and size at metamorphosis in laboratory-reared individuals of the freshwater copepod, Diaptomus leptopus , and then followed individuals over their entire life cycle to assess the fitness consequences of variation in age and size at metamorphosis. In 3 separate experiments, individuals were raised in different food conditions: low food (0.2 μg C/ml) switched to high food (0.7 μg C/ml), or high food switched to low food, at several different larval and juvenile stages. Control individuals were reared on high or low food concentrations over their entire life cycles. For each individual, we measured age and size at metamorphosis and age and size at maturity; for females, we also measured total lifetime egg production, longevity, and calculated a composite fitness measure, λ. Statistical analyses showed no significant effects of age or size at metamorphosis on these same traits measured at maturity, or on the fitness components we estimated. The first individuals to mature had the highest total egg production and individual fitness; differences in body size at maturation explained none of the variation observed in fitness components. Our results show that metamorphosis was uncoupled from maturity and from fitness components by growth and development achieved during the juvenile phase of the life cycle, and support the conclusion that fitness consequences of metamorphosis depend fundamentally on the organization of an organism's life cycle. They also suggest that body size plays a different life-history role in these organisms than is recognized in most poikilotherms, and suggest the hypothesis, based on laboratory experiments, that selection may act primarily on juvenile developmental rates in field populations.     

The evolution of parental care in insects: A test of current hypotheses

Which sex should care for offspring is a fundamental question in evolution. Invertebrates, and insects in particular, show some of the most diverse kinds of parental care of all animals, but to date there has been no broad comparative study of the evolution of parental care in this group. Here, we test existing hypotheses of insect parental care evolution using a literature‐compiled phylogeny of over 2000 species. To address substantial uncertainty in the insect phylogeny, we use a brute force approach based on multiple random resolutions of uncertain nodes. The main transitions were between no care (the probable ancestral state) and female care. Male care evolved exclusively from no care, supporting models where mating opportunity costs for caring males are reduced—for example, by caring for multiple broods—but rejecting the “enhanced fecundity” hypothesis that male care is favored because it allows females to avoid care costs. Biparental care largely arose by males joining caring females, and was more labile in Holometabola than in Hemimetabola. Insect care evolution most closely resembled amphibian care in general trajectory. Integrating these findings with the wealth of life history and ecological data in insects will allow testing of a rich vein of existing hypotheses.