Annelids in evolutionary developmental biology and comparative genomics

Annelids have had a long history in comparative embryology and morphology, which has helped to establish them in zoology textbooks as an ideal system to understand the evolution of the typical triploblastic, coelomate, protostome condition. In recent years there has been a relative upsurge in embryological data, particularly with regard to the expression and function of developmental control genes. Polychaetes, as well as other annelids such as the parasitic leech, are now also entering the age of comparative genomics. All of this comparative data has had an important impact on our views of the ancestral conditions at various levels of the animal phylogeny, including the bilaterian ancestor and the nature of the annelid ancestor. Here we review some of the recent advances made in annelid comparative development and genomics, revealing a hitherto unsuspected level of complexity in these ancestors. It is also apparent that the transition to a parasitic lifestyle leads to, or requires, extensive modifications and derivations at both the genomic and embryological levels.     

Life history evolution and demographic stochasticity

Summary Can demographic stochasticity bias the evolution of life history traits? Under a neutral version of the Cole-Charnov-Schaffer model, variance in offspring number for both annuals and perennials depends on the precise values of fitness components. Either annuals or perennials may have the larger variance (for equal ), depending on the importance of random survivalversus fixed reproduction. By extension, the variance in offspring number should generally depend on whether is mainly composed of highly variable elements or elements with limited variation. Thus, data about the variability of demographic parameters may be as important as data about their mean values.This result concerns only one source of demographic stochasticity, the probabilistic nature of demographic processes like survival. The other source of demographic stochasticity is the fact that populations are composed of whole numbers of individuals (integer arithmetic). Integer arithmetic without probabilistic demography (or environmental variation) can make it difficult for rare invaders to persist in populations even when selection would favour the invaders in a deterministic model. Integer arithmetic can also cause population coexistence when the equivalent deterministic model leads to exclusion. This effect disappears when demography is probabilistic, and probably also when there is environmental variation. Thus probabilistic demography and environmental variation may make some population patterns more, rather than less, understandable.     

Primate comparative genomics: lemur biology and evolution

Comparative genome sequencing projects are providing insight into aspects of genome biology that raise new questions and challenge existing paradigms. Placement in the phylogenetic tree can often be a major determinant of which organism to choose for study. Lemurs hold a key position at the base of the primate evolutionary tree and will be highly informative for the genomics community by offering comparisons of primate-specific characteristics and processes. Combining research in chromosome evolution, genome evolution and behavior with lemur comparative genomic sequencing will offer insights into many levels of primate evolution. We discuss the current state of lemur cytogenetic and phylogenetic analyses, and suggest how focusing more genomic efforts on lemurs will be beneficial to understanding human and primate evolution, as well as disease, and will contribute to conservation efforts.     

Planarian embryology in the era of comparative developmental biology

During the last decade, the field of evolutionary developmental biology (evo-devo) has emerged as a major research discipline in modern biology and an essential approach to understanding evolutionary relationships in the animal kingdom. At the same time, planarians have become a useful and important model with which to address basic questions regarding the molecular and cellular basis of regeneration, tissue repair and stem cells in adult organisms. Nevertheless, little attention has been paid to their embryonic development, even though this provides a unique opportunity for studying how molecular developmental mechanisms are re-deployed during adult regeneration or the independent losses of spiral cleavage that took place in different lophotrochozoan lineages. In this paper, we review the most relevant works on planarian embryos from a historical point of view. In doing so, we highlight the questions that have recurrently intrigued researchers, most of which remain unanswered. Finally, we present a comprehensive scenario for planarian embryogenesis in an attempt to provide a testable hypothesis that will help to bridge the gap between this divergent mode of development, the ancestral canonical spiral cleavage, and adult planarian regeneration.     

Life history and the evolution of human maturation

The Taung child, like fossils of other individuals who died before reaching adulthood, is a piece of the puzzle of the evolution of human growth and development, the puzzle of when, how, and why human “life history” evolved into its modern form. With regard to Taung, interest focuses on both its rate of growth (maturation of the child in relation to its age) and its pattern of growth (synchrony of the elements of maturation). The meaning of rates and patterns of growth, as well as the interpretation of maturation of Taung or any other fossil mammal, are best understood through the broad perspectives provided by comparative study of mammalian life history and the techniques of allometry.     

Homology and ontogeny: pattern and process in comparative developmental biology

In this article the interface between development and homology is discussed. Development is here interpreted as a sequence of evolutionarily independent stages. Any approach stressing the importance of specific developmental stages is rejected. A homology definition is favoured which includes similarity, and complexity serves as a test for homology. Complexity is seen as the possibility of subdividing a character into evolutionarily independent corresponding substructures. Topology as a test for homology is critically discussed because corresponding positions are not necessarily indicative of homology. Complexity can be used twofold for homology assessments of development: either stages or processes of development are homologised. These two approaches must not be conflated. This distinction leads to the conclusion that there is no ontogenetic homology “criterion”.     

Life history diversity and evolution in the Asterinidae

Asterinid sea stars have the greatest range of life historiesknown for the Asteroidea. Larval form in these sea stars hasbeen modified in association with selection for planktonic,benthic, or intergonadal developmental habitats. Life historydata are available for 31 species and molecular data for 28of these. These data were used to assess life history evolutionand relationships among asterinid clades. Lecithotrophy is prevalentin Asterinidae, with at least 6 independent origins of thisdevelopmental mode. Morphological differences in the attachmentcomplex of brachiolaria larvae were evident among species withplanktonic lecithotrophy. Some features are clade specific whileothers are variable within clades. Benthic brachiolariae aresimilar in Aquilonastra and Parvulastra with tripod-shaped larvae,while the bilobed sole-shaped larvae of Asterina species appearunique to this genus. Multiple transitions and pathways havebeen involved in the evolution of lecithotropy in the Asterinidae.Although several genera have a species with a planktonic feedinglarva in a basal phylogenetic position, relative to specieswith planktonic or benthic lecithotrophy, there is little evidencefor the expected life history transformation series from planktonicfeeding, to planktonic non-feeding, to benthic non-feeding development.Intragonadal development, a life history pattern unique to theAsterinidae, arose three times through ancestors with benthicor pelagic lecithotrophy. Evolution of lecithotrophy appearsmore prevalent in the Asterinidae than other asteroid families.As diverse modes of development are discerned in cryptic speciescomplexes, new insights into life history evolution in the Asterinidaeare being generated.     

Life history evolution with antagonistic pleiotropy and overlapping generations

Previous results found for selection with antagonistic pleiotropy and discrete generations are extended to cases with overlapping generations. In order to do so, protected polymorphism conditions are found for monoecious and dioecious populations when the intrinsic rate of increase, or Malthusian parameter, is not too large in magnitude. Under such conditions, it is shown that recessive deleterious gene effects foster the maintenance of allelic variants affecting life history. The significance of this result for experimental studies of the evolution of senescence is addressed.     

Convergent maternal provisioning and life-history evolution in echinoderms

In marine invertebrates, the frequent evolution of lecithotrophic nonfeeding development from a planktotrophic feeding ancestral developmental mode has involved the repeated, independent acquisition of a large, lipid-rich, usually buoyant egg. To investigate the mechanistic basis of egg-size evolution and the role of maternally provisioned lipids in lecithotrophic development, we identified and quantified the egg lipids in six sea urchin species and five sea star species encompassing four independent evolutionary transformations to lecithotrophy. The small eggs of species with planktotrophic development were dominated by triglycerides with low levels of wax esters, whereas the larger eggs of lecithotrophs contain measurable triglycerides but were dominated by wax ester lipids, a relatively minor egg component of planktotrophs. Comparative analysis by independent contrasts confirmed that after removing the influence of phylogeny, the evolution of a large egg by lecithotrophs was correlated with the conspicuous deposition of wax esters. Increases in wax ester abundance exceeded expectations based solely on changes in egg volume. Wax esters may have roles in providing buoyancy to the egg and for postmetamorphic provisioning. Experimentally reducing the amount of wax esters in blastula stage embryos of the lecithotroph Heliocidaris erythrogramma resulted in a viable but nonbuoyant larvae. During normal development for H. erythrogramma, wax ester biomass remained constant during development to metamorphosis (five days postfertilization), but decreased during juvenile development before complete mouth formation (12 days postfertilization) and was further reduced at 18 days postfertilization. The function of wax esters may be specific to the lecithotrophic developmental mode because there were negligible wax esters present in competent pluteus larvae of Strongylocentrotus drobachiensis, a planktotrophic species. These data suggest that this seminal evolutionary modification, the production of a large egg, has been accomplished in part by the elaboration of a preexisting oogenic component, wax esters. The modification of preexisting oogenic processes may facilitate the observed high frequency of transformations in larval mode in marine invertebrates.     

Diversity dynamics of echinoderms and evolution of marine communities

A compound analysis of two global paleontological databases (Sepkoski??s database (SDB) and The Paleobiology Database) allowed the recognition of a number of previously undescribed trends in the evolution of the phylum Echinodermata. Paleozoic echinoderms, dominated by sessile epibenthic filter feeders, played an important role in benthic communities, especially in the Ordovician and Carboniferous. Paleozoic echinoderms typically showed an increased rate of genus renewal, which significantly decreases in the Meso-Cenozoic. After the P-T crisis the echinoderms became dominated by motile taxa, while the role of infaunal forms increased. During the global turnover in the benthic communities at the K-T boundary, which was accompanied by a sharp increase in the mean alpha-diversity, many marine organisms became inhabitants of much richer (compared to the Mesozoic) communities. However, of all echinoderms, this trend is observed only in crinoids. In contrast to most large taxa, echinoderms do not show positive correlation between the duration of genera and alpha-diversity of communities, which included these genera. During the Phanerozoic the geographical distribution of echinoderms showed a sharp paleolatitudinal gradient, i.e., each period was characterized by one paleolatitudinal zone with the maximum diversity of echinoderms, and the diversity rapidly decreasing to the north and to the south of this zone. The zone of the maximum diversity of echinoderms, like of entire marine biota, during the Phanerozoic gradually moved from the tropics of the southern hemisphere to the middle latitudes of the northern hemisphere.     

Life history and developmental processes in the basidiomycete Coprinus cinereus.

Coprinus cinereus has two main types of mycelia, the asexual monokaryon and the sexual dikaryon, formed by fusion of compatible monokaryons. Syngamy (plasmogamy) and karyogamy are spatially and temporally separated, which is typical for basidiomycetous fungi. This property of the dikaryon enables an easy exchange of nuclear partners in further dikaryotic-monokaryotic and dikaryotic-dikaryotic mycelial fusions. Fruiting bodies normally develop on the dikaryon, and the cytological process of fruiting-body development has been described in its principles. Within the specialized basidia, present within the gills of the fruiting bodies, karyogamy occurs in a synchronized manner. It is directly followed by meiosis and by the production of the meiotic basidiospores. The synchrony of karyogamy and meiosis has made the fungus a classical object to study meiotic cytology and recombination. Several genes involved in these processes have been identified. Both monokaryons and dikaryons can form multicellular resting bodies (sclerotia) and different types of mitotic spores, the small uninucleate aerial oidia, and, within submerged mycelium, the large thick-walled chlamydospores. The decision about whether a structure will be formed is made on the basis of environmental signals (light, temperature, humidity, and nutrients). Of the intrinsic factors that control development, the products of the two mating type loci are most important. Mutant complementation and PCR approaches identified further genes which possibly link the two mating-type pathways with each other and with nutritional regulation, for example with the cAMP signaling pathway. Among genes specifically expressed within the fruiting body are those for two galectins, beta-galactoside binding lectins that probably act in hyphal aggregation. These genes serve as molecular markers to study development in wild-type and mutant strains. The isolation of genes for potential non-DNA methyltransferases, needed for tissue formation within the fruiting body, promises the discovery of new signaling pathways, possibly involving secondary fungal metabolites.     

Life history and the evolution of family living in birds

The reason why some bird species live in family groups is an important question of evolutionary biology that remains unanswered. Families arise when young delay the onset of independent reproduction and remain with their parents beyond independence. Explanations for why individuals forgo independent reproduction have hitherto focused on dispersal constraints, such as the absence of high-quality breeding openings. However, while constraints successfully explain within-population dispersal decisions, they fail as an ultimate explanation for variation in family formation across species. Most family-living species are long-lived and recent life-history studies demonstrated that a delayed onset of reproduction can be adaptive in long-lived species. Hence, delayed dispersal and reproduction might be an adaptive life-history decision rather than 'the best of a bad job'. Here, we attempt to provide a predictive framework for the evolution of families by integrating life-history theory into family formation theory. We suggest that longevity favours a delayed onset of reproduction and gives parents the opportunity of a prolonged investment in offspring, an option which is not available for short-lived species. Yet, parents should only prolong their investment in offspring if this increases offspring survival and outweighs the fitness cost that parents incur, which is only possible under ecological conditions, such as a predictable access to resources. We therefore propose that both life-history and ecological factors play a role in determining the evolution of family living across species, yet we suggest different mechanisms than those proposed by previous models.     

Phosphagen kinase evolution. Expression in echinoderms

Arginine kinase and creatine kinase that catalyze the transfer of a phosphate group between ATP and arginine and creatine, respectively, play an important role in cellular energetics. In contrast to most animals which exhibit a single phosphagen kinase activity (creatine kinase in chordates and arginine kinase in protostomians), echinoderms exhibit both arginine kinase and creatine kinase activities, sometimes in the same tissue. In contrast to chordates in which creatine kinases are dimers (consisting of two subunits of 40 kDa) and protostomians in which arginine kinases are usually monomers (40 kDa), echinoids contain specific phosphagen kinases: a dimeric arginine kinase (consisting of two subunits of 42 kDa) in eggs and a monomeric creatine kinase (145 kDa) in sperm. We have examined echinoderms from the five existing classes (echinoids, asteroids, ophiuroids, holothurians and crinoids) for the expression of these specific phosphagen kinases in different tissues. Gel filtration was used to determine the molecular masses of the native enzymes. Antibodies specific for arginine kinase or for creatine kinase were used to characterize the subunit composition of arginine kinase and creatine kinase after SDS/PAGE and transfer. In all echinoderms analyzed, arginine kinase always occurred as an enzyme of about 81 kDa consisting of two subunits of 42 kDa and creatine kinase as a monomeric enzyme of 140-155 kDa. The occurrence in echinoderms of both phosphagen kinases with distinct specificities and specific molecular structures is discussed from both a developmental and evolutionary point of view.     

Life history and development--a framework for understanding developmental plasticity in lower termites

Termites (Isoptera) are the phylogenetically oldest social insects, but in scientific research they have always stood in the shadow of the social Hymenoptera. Both groups of social insects evolved complex societies independently and hence, their different ancestry provided them with different life-history preadaptations for social evolution. Termites, the 'social cockroaches', have a hemimetabolous mode of development and both sexes are diploid, while the social Hymenoptera belong to the holometabolous insects and have a haplodiploid mode of sex determination. Despite this apparent disparity it is interesting to ask whether termites and social Hymenoptera share common principles in their individual and social ontogenies and how these are related to the evolution of their respective social life histories. Such a comparison has, however, been much hampered by the developmental complexity of the termite caste system, as well as by an idiosyncratic terminology, which makes it difficult for non-termitologists to access the literature.
Here, we provide a conceptual guide to termite terminology based on the highly flexible caste system of the "lower termites". We summarise what is known about ultimate causes and underlying proximate mechanisms in the evolution and maintenance of termite sociality, and we try to embed the results and their discussion into general evolutionary theory and developmental biology. Finally, we speculate about fundamental factors that might have facilitated the unique evolution of complex societies in a diploid hemimetabolous insect taxon. This review also aims at a better integration of termites into general discussions on evolutionary and developmental biology, and it shows that the ecology of termites and their astounding phenotypic plasticity have a large yet still little explored potential to provide insights into elementary evo-devo questions.     

Life history evolution in Lodoicea maldivica (Arecaceae)

Lodoicea maldivica , a palm endemic to two small islands in the Seychelles group, has the largest seed in the plant kingdom. We present here an interpretation of the ecological and evolutionary significance of this seed in terms of the island environment where the species grows. We begin by reviewing the available information about the biology and ecology of Lodoicea and present some original data on the growth and development of Lodoicea in its native habitat. A remarkable feature of young plants is the enormous size of their leaves and the great length of their petioles, these being especially elongated when growing beneath the canopy. As a result, juvenile plants can reach a height of 15 m and hold their foliage in the forest canopy. This capacity to produce such an enormous juvenile plant is related in part to the large food reserves in the seed. We suggest that Lodoicea evolved from a more typical borassoid palm (perhaps a plant like Borassus aethiopum which is widespread in the savannas of Africa) and propose two hypotheses to explain why this occurred. According to the 'shade hypothesis', increasingly humid conditions on the Seychelles led to strong selection for plants with the tallest seedlings, since these would be the most likely to establish successfully under the low light conditions prevailing on the forest floor of closed forest. The 'sibling competition hypothesis' postulates that the island populations of the ancestral palm lost any means for seed dispersal, and their seeds simply fell to the foot of the parent tree. This resulted in a strong selection pressure for reduced fecundity. The two hypotheses are not mutually exclusive, and together they may help us to understand many of the unusual features of this remarkable species.     

How development changes evolution: conceptual and historical issues in evolutionary developmental biology

Evolutionary developmental biology (Evo-Devo) is a new and rapidly developing field of biology which focuses on questions in the intersection of evolution and development and has been seen by many as a potential synthesis of these two fields. This synthesis is the topic of the books reviewed here. Integrating Evolution and Development (edited by Roger Sansom and Robert Brandon), is a collection of papers on conceptual issues in Evo-Devo, while From Embryology to Evo-Devo (edited by Manfred Laubichler and Jane Maienschein) is a history of the problem of the relations between ontogeny and phylogeny.