Developmental modularity and phenotypic novelty within a biphasic life cycle: morphogenesis of a cone snail venom gland

The venom gland of predatory cone snails (Conus spp.), which secretes neurotoxic peptides that rapidly immobilize prey, is a proposed key innovation for facilitating the extraordinary feeding behaviour of these gastropod molluscs. Nevertheless, the unusual morphology of this gland has generated controversy about its evolutionary origin and possible homologues in other gastropods. I cultured feeding larvae of Conus lividus and cut serial histological sections through the developing foregut during larval and metamorphic stages to examine the development of the venom gland. Results support the hypothesis of homology between the venom gland and the mid-oesophageal gland of other gastropods. They also suggest that the mid-region of the gastropod foregut, like the anterior region, is divisible into dorsal and ventral developmental modules that have different morphological, functional and ontogenetic fates. In larvae of C. lividus, the ventral module of the middle foregut transformed into the anatomically novel venom gland of the post-metamorphic stage by rapidly pinching-off from the main dorsal channel of the mid-oesophagus, an epithelial remodelling process that may be similar to other cases where epithelial tubes and vesicles arise from a pre-existing epithelial sheet. The developmental remodelling mechanism could have facilitated an abrupt evolutionary transition to the derived morphology of this important gastropod feeding innovation.     

The evolutionary origins of patriarchy

This article argues that feminist analyses of patriarchy should be expanded to address the evolutionary basis of male motivation to control female sexuality. Evidence from other primates of male sexual coercion and female resistance to it indicates that the sexual conflicts of interest that underlie patriarchy predate the emergence of the human species. Humans, however, exhibit more extensive male dominance and male control of female sexuality than is shown by most other primates. Six hypotheses are proposed to explain how, over the course of human evolution, this unusual degree of gender inequality came about. This approach emphasizes behavioral flexibility, cross-cultural variability in the degree of partriarchy, and possibilities for future change. This work was supported in part by NSF grant BNS-8857969. Barbara Smuts is a professor of psychology and anthropology at the University of Michigan. She received her B.A. in social anthropology at Harvard and her Ph.D. in bio-behavioral sciences at Stanford Medical School. She has studied the behavior of wild chimpanzees, baboons, and bottlenose dolphins and is particularly interested in evolutionary, comparative analyses of female-male relationships.     

Toward a universal measure of robustness across model organs and systems

The development of an individual must be capable of resisting the harmful effects of internal and external perturbations. This capacity, called robustness, can make the difference between normal variation and disease. Some systems and organs are more resilient in their capacity to correct the effects of internal disturbances such as mutations. Similarly, organs and organisms differ in their capacity to be resilient against external disturbances, such as changes in temperature. Furthermore, all developmental systems must be somewhat flexible to permit evolutionary change, and understanding robustness requires a comparative framework. Over the last decades, most research on developmental robustness has been focusing on specific model systems and organs. Hence, we lack tools that would allow cross-species and cross-organ comparisons. Here, we emphasize the need for a uniform framework to experimentally test and quantify robustness across study systems and suggest that the analysis of fluctuating asymmetry might be a powerful proxy to do so. Such a comparative framework will ultimately help to resolve why and how organs of the same and different species differ in their sensitivity to internal (e.g., mutations) and external (e.g., temperature) perturbations and at what level of biological organization buffering capacities exist and therefore create robustness of the developmental system.     

Ecological,historical and evolutionary determinants of modularity in weighted seed‐dispersal networks

Modularity is a recurrent and important property of bipartite ecological networks. Although well‐resolved ecological networks describe interaction frequencies between species pairs, modularity of bipartite networks has been analysed only on the basis of binary presence–absence data. We employ a new algorithm to detect modularity in weighted bipartite networks in a global analysis of avian seed‐dispersal networks. We define roles of species, such as connector values, for weighted and binary networks and associate them with avian species traits and phylogeny. The weighted, but not binary, analysis identified a positive relationship between climatic seasonality and modularity, whereas past climate stability and phylogenetic signal were only weakly related to modularity. Connector values were associated with foraging behaviour and were phylogenetically conserved. The weighted modularity analysis demonstrates the dominating impact of ecological factors on the structure of seed‐dispersal networks, but also underscores the relevance of evolutionary history in shaping species roles in ecological communities.     

Functional integration for enrolment constrains evolutionary variation of phacopid trilobites despite developmental modularity

Modularity and integration are variational properties expressed at various levels of the biological hierarchy. Mismatches among these levels, for example developmental modules that are integrated in a functional unit, could be informative of how evolutionary processes and trade‐offs have shaped organismal morphologies as well as clade diversification. In the present study, we explored the full, integrated and modular spaces of two developmental modules in phacopid trilobites, the cephalon and the pygidium, and highlight some differences among them. Such contrasts reveal firstly that evolutionary processes operating in the modular spaces are stronger in the cephalon, probably due to a complex regime of selection related to the numerous functions ensured by this module. Secondly, we demonstrate that the same pattern of covariation is shared among species, which also differentiate along this common functional integration. This common pattern might be the result of stabilizing selection acting on the enrolment and implying a coordinate variation between the cephalon and the pygidium in a certain direction of the morphospace. Finally, we noticed that Austerops legrandi differs slightly from other species in that its integration is partly restructured in the way the two modules interact. Such a divergence can result from the involvement of the cephalon in several vital functions that may have constrained the response of the features involved in enrolment and reorganized the covariation of the pygidium with the cephalon. Therefore, it is possible that important evolutionary trade‐offs between enrolment and other functions on the cephalon might have partly shaped the diversification of trilobites.     

Chimeric dihydrofolate reductases display properties of modularity and biophysical diversity

While reverse genetics and functional genomics have long affirmed the role of individual mutations in determining protein function, there have been fewer studies addressing how large‐scale changes in protein sequences, such as in entire modular segments, influence protein function and evolution. Given how recombination can reassort protein sequences, these types of changes may play an underappreciated role in how novel protein functions evolve in nature. Such studies could aid our understanding of whether certain organismal phenotypes related to protein function—such as growth in the presence or absence of an antibiotic—are robust with respect to the identity of certain modular segments. In this study, we combine molecular genetics with biochemical and biophysical methods to gain a better understanding of protein modularity in dihydrofolate reductase (DHFR), an enzyme target of antibiotics also widely used as a model for protein evolution. We replace an integral α‐helical segment of Escherichia coli DHFR with segments from a number of different organisms (many nonmicrobial) and examine how these chimeric enzymes affect organismal phenotypes (e.g., resistance to an antibiotic) as well as biophysical properties of the enzyme (e.g., thermostability). We find that organismal phenotypes and enzyme properties are highly sensitive to the identity of DHFR modules, and that this chimeric approach can create enzymes with diverse biophysical characteristics.     

Multilevel assessment of the Lacertid lizard cranial modularity

Different factors and processes that produce phenotypic variation at the individual, population, or interspecific level can influence or alter the covariance structure among morphological traits. Therefore, studies of the patterns of integration and modularity at multiple levels—static, ontogenetic, and evolutionary, can provide invaluable data on underlying factors and processes that structured morphological variation, directed, or constrained evolutionary changes. Our dataset, consisting of cranium shape data for 14 lizard species from the family Lacertidae, with substantial samples of hatchlings and adults along with their inferred evolutionary relationships, enabled us to assess modularity and morphological integration at all three levels. Five, not mutually exclusive modularity hypotheses of lizard cranium, were tested, and the effects of allometry on intensity and the pattern of integration and modularity were estimated. We used geometric morphometrics to extract symmetric and asymmetric, as well as allometric and nonallometric, components of shape variation. At the static level, firm confirmation of cranial modularity was found for hypotheses which separate anterior and posterior functional compartments of the skull. At the ontogenetic level, two alternative hypotheses (the “anteroposterior” and “neurodermatocranial” hypotheses) of ventral cranial modularity were confirmed. At the evolutionary level, the “neurodermatocranial” hypothesis was confirmed for the ventral cranium, which is in accordance with the pattern observed at the ontogenetic level. The observed pattern of static modularity could be driven by functional demands and can be regarded as adaptive. Ontogenetic modularity and evolutionary modularity show the same developmental origin, indicating conservatism of modularity patterns driven by developmental constraints.     

The evolutionary origins and catalytic importance of conserved electrostatic networks within TIM-barrel proteins

Conservation of function is the basic tenet of protein evolution. Conservation of key electrostatic properties is a frequently employed mechanism that leads to conserved function. In a previous report, we identified several conserved electrostatic properties in four protein families and one functionally diverse enzyme superfamily. In this report, we demonstrate the evolutionary and catalytic importance of electrostatic networks in three ubiquitous metabolic enzymes: triosephosphate isomerase, enolase, and transaldolase. Evolutionary importance is demonstrated using phylogenetic motifs (sequence fragments that parallel the overall familial phylogeny). Phylogenetic motifs frequently correspond to both catalytic residues and conserved interactions that fine-tune catalytic residue pKa values. Further, in the case of triosephosphate isomerase, quantitative differences in the catalytic Glu169 pKa values parallel subfamily differentiation. Finally, phylogenetic motifs are shown to structurally cluster around the active sites of eight different TIM-barrel families. Depending upon the mechanistic requisites of each reaction catalyzed, interruptions to the canonical fold may or may not be identified as phylogenetic motifs.     

A test for patterns of modularity in sequences of developmental events

This study presents a statistical test for modularity in the context of relative timing of developmental events. The test assesses whether sets of developmental events show special phylogenetic conservation of rank order. The test statistic is the correlation coefficient of developmental ranks of the N events of the hypothesized module across taxa. The null distribution is obtained by taking correlation coefficients for randomly sampled sets of N events. This test was applied to two datasets, including one where phylogenetic information was taken into account. The events of limb development in two frog species were found to behave as a module.     

Predicting evolutionary potential: A numerical test of evolvability measures

Despite sophisticated mathematical models, the theory of microevolution is mostly treated as a qualitative rather than a quantitative tool. Numerical measures of selection, constraints, and evolutionary potential are often too loosely connected to theory to provide operational predictions of the response to selection. In this paper, we study the ability of a set of operational measures of evolvability and constraint to predict short‐term selection responses generated by individual‐based simulations. We focus on the effects of selective constraints under which the response in one trait is impeded by stabilizing selection on other traits. The conditional evolvability is a measure of evolutionary potential explicitly developed for this situation. We show that the conditional evolvability successfully predicts rates of evolution in an equilibrium situation, and further that these equilibria are reached with characteristic times that are inversely proportional to the fitness load generated by the constraining characters. Overall, we find that evolvabilities and conditional evolvabilities bracket responses to selection, and that they together can be used to quantify evolutionary potential on time scales where the G‐matrix remains relatively constant.     

The evolvability of herkogamy: Quantifying the evolutionary potential of a composite trait

Accurate estimates of trait evolvabilities are central to predicting the short‐term evolutionary potential of populations, and hence their ability to adapt to changing environments. We quantify and evaluate the evolvability of herkogamy, the spatial separation of male and female structures in flowers, a key floral trait associated with variation in mating systems. We compiled genetic‐variance estimates for herkogamy and related floral traits, computed evolvabilities, and compared these among trait groups and among species differing in their mating systems. When measured in percentage of its own size, the median evolvability of herkogamy was an order of magnitude greater than the evolvability of other floral size measurements, and was generally not strongly constrained by genetic covariance between its components (pistil and stamen lengths). Median evolvabilities were similar across mating systems, with only a tendency toward reduction in highly selfing taxa. We conclude that herkogamy has the potential to evolve rapidly in response to changing environments. This suggests that the extensive variation in herkogamy commonly observed among closely related populations and species may result from rapid adaptive tracking of fitness optima determined by variation in pollinator communities or other selective factors.     

The role of epiphytism in architecture and evolutionary constraint within mycorrhizal networks of tropical orchids

Characterizing the architecture of bipartite networks is increasingly used as a framework to study biotic interactions within their ecological context and to assess the extent to which evolutionary constraint shape them. Orchid mycorrhizal symbioses are particularly interesting as they are viewed as more beneficial for plants than for fungi, a situation expected to result in an asymmetry of biological constraint. This study addressed the architecture and phylogenetic constraint in these associations in tropical context. We identified a bipartite network including 73 orchid species and 95 taxonomic units of mycorrhizal fungi across the natural habitats of Reunion Island. Unlike some recent evidence for nestedness in mycorrhizal symbioses, we found a highly modular architecture that largely reflected an ecological barrier between epiphytic and terrestrial subnetworks. By testing for phylogenetic signal, the overall signal was stronger for both partners in the epiphytic subnetwork. Moreover, in the subnetwork of epiphytic angraecoid orchids, the signal in orchid phylogeny was stronger than the signal in fungal phylogeny. Epiphytic associations are therefore more conservative and may co‐evolve more than terrestrial ones. We suggest that such tighter phylogenetic specialization may have been driven by stressful life conditions in the epiphytic niches. In addition to paralleling recent insights into mycorrhizal networks, this study furthermore provides support for epiphytism as a major factor affecting ecological assemblage and evolutionary constraint in tropical mycorrhizal symbioses.     

Robustness and evolvability: a paradox resolved

Understanding the relationship between robustness and evolvability is key to understand how living things can withstand mutations, while producing ample variation that leads to evolutionary innovations. Mutational robustness and evolvability, a system's ability to produce heritable variation, harbour a paradoxical tension. On one hand, high robustness implies low production of heritable phenotypic variation. On the other hand, both experimental and computational analyses of neutral networks indicate that robustness enhances evolvability. I here resolve this tension using RNA genotypes and their secondary structure phenotypes as a study system. To resolve the tension, one must distinguish between robustness of a genotype and a phenotype. I confirm that genotype (sequence) robustness and evolvability share an antagonistic relationship. In stark contrast, phenotype (structure) robustness promotes structure evolvability. A consequence is that finite populations of sequences with a robust phenotype can access large amounts of phenotypic variation while spreading through a neutral network. Population-level processes and phenotypes rather than individual sequences are key to understand the relationship between robustness and evolvability. My observations may apply to other genetic systems where many connected genotypes produce the same phenotypes.     

The evolutionary origins of pesticide resistance

Durable crop protection is an essential component of current and future food security. However, the effectiveness of pesticides is threatened by the evolution of resistant pathogens, weeds and insect pests. Pesticides are mostly novel synthetic compounds, and yet target species are often able to evolve resistance soon after a new compound is introduced. Therefore, pesticide resistance provides an interesting case of rapid evolution under strong selective pressures, which can be used to address fundamental questions concerning the evolutionary origins of adaptations to novel conditions. We ask: (i) whether this adaptive potential originates mainly from de novo mutations or from standing variation; (ii) which pre‐existing traits could form the basis of resistance adaptations; and (iii) whether recurrence of resistance mechanisms among species results from interbreeding and horizontal gene transfer or from independent parallel evolution. We compare and contrast the three major pesticide groups: insecticides, herbicides and fungicides. Whilst resistance to these three agrochemical classes is to some extent united by the common evolutionary forces at play, there are also important differences. Fungicide resistance appears to evolve, in most cases, by de novo point mutations in the target‐site encoding genes; herbicide resistance often evolves through selection of polygenic metabolic resistance from standing variation; and insecticide resistance evolves through a combination of standing variation and de novo mutations in the target site or major metabolic resistance genes. This has practical implications for resistance risk assessment and management, and lessons learnt from pesticide resistance should be applied in the deployment of novel, non‐chemical pest‐control methods.     

The evolutionary role of modularity and integration in the hominoid cranium

Patterns of morphological integration and modularity among shape features emerge from genetic and developmental factors with varying pleiotropic effects. Factors or processes affecting morphology only locally may respond to selection more easily than common factors that may lead to deleterious side effects and hence are expected to be more conserved. We briefly review evidence for such global factors in primate cranial development as well as for local factors constrained to either the face or the neurocranium. In a sample comprising 157 crania of Homo sapiens, Pan troglodytes, and Gorilla gorilla, we statistically estimated common and local factors of shape variation from Procrustes coordinates of 347 landmarks and semilandmarks. Common factors with pleiotropic effects on both the face and the neurocranium account for a large amount of shape variation, but mainly by extension or truncation of otherwise conserved developmental pathways. Local factors (modular shape characteristics) have more degrees of freedom for evolutionary change than mere ontogenetic scaling. Cranial shape is similarly integrated during development in all three species, but human evolution involves dissociation among several characteristics. The dissociation has probably been achieved by evolutionary alterations and by the novel emergence of local factors affecting characteristics that are controlled at the same time by the common factors.     

The origins and evolutionary expansion of the Strongylida (Nematoda)

The Strongylida are thought to have arisen from free-living rhabditoid nematodes, but the relationships between the major groupings within the Strongylida, the Strongylina, the Metastrongylina, Trichostrongylina and the Ancylostomatina are far from clear in spite of the abundance of morphological data now available for analysis. Evolutionary mechanisms including co-evolution, host switching, host dispersal, use of intermediate hosts, various sites of localisation within the definitive host and modifications of life-cycle strategies appear to have been utilised in the expansion of the Strongylida, with different mechanisms predominating in different families or superfamilies. Co-evolution appears to have been a major mode of evolution in the Strongylina, in contrast to the Trichostrongylina, which have used host dispersal and host-switching to great advantage. The phylogeny of the Ancylostomatina shows little association with host evolution, but does match the feeding preferences of the hosts. The Metastrongylina have utilised intermediate hosts and life cycle modifications including a shift to extra-intestinal sites as major means of diversification, in contrast to the other sub-orders. The review, while indicating much progress in our understanding of the phylogeny of the Strongylida, also reveals that enormous gaps still exist, and emphasises the tentative nature of many of the phylogenetic hypotheses tendered to date.     

The evolutionary dynamics of evolvability in a gene network model

Evolvability, the ability of populations to adapt, has recently emerged as a major unifying concept in biology. Although the study of evolvability offers new insights into many important biological questions, the conceptual bases of evolvability, and the mechanisms of its evolution, remain controversial. We used simulated evolution of a model of gene network dynamics to test the contentious hypothesis that natural selection can favour high evolvability, in particular in sexual populations. Our results conclusively demonstrate that fluctuating natural selection can increase the capacity of model gene networks to adapt to new environments. Detailed studies of the evolutionary dynamics of these networks establish a broad range of validity for this result and quantify the evolutionary forces responsible for changes in evolvability. Analysis of the genotype–phenotype map of these networks also reveals mechanisms connecting evolvability, genetic architecture and robustness. Our results suggest that the evolution of evolvability can have a pervasive influence on many aspects of organisms.     

Studying morphological integration and modularity at multiple levels: concepts and analysis

Although most studies on integration and modularity have focused on variation among individuals within populations or species, this is not the only level of variation for which integration and modularity exist. Multiple levels of biological variation originate from distinct sources: genetic variation, phenotypic plasticity resulting from environmental heterogeneity, fluctuating asymmetry from random developmental variation and, at the interpopulation or interspecific levels, evolutionary change. The processes that produce variation at all these levels can impart integration or modularity on the covariance structure among morphological traits. In turn, studies of the patterns of integration and modularity can inform about the underlying processes. In particular, the methods of geometric morphometrics offer many advantages for such studies because they can characterize the patterns of morphological variation in great detail and maintain the anatomical context of the structures under study. This paper reviews biological concepts and analytical methods for characterizing patterns of variation and for comparing across levels. Because research comparing patterns across level has only just begun, there are relatively few results, generalizations are difficult and many biological and statistical questions remain unanswered. Nevertheless, it is clear that research using this approach can take advantage of an abundance of new possibilities that are so far largely unexplored.