“Indirect development” increases reproductive plasticity and contributes to the success of scyphozoan jellyfish in the oceans

Ecologists and evolutionary biologists have been looking for the key(s) to the success of scyphomedusae through their long evolutionary history in multiple habitats. Their ability to generate young medusae (ephyrae) via two distinct reproductive strategies, strobilation or direct development from planula into ephyra without a polyp stage, has been a potential explanation. In addition to these reproductive modes, here we provide evidence of a third ephyral production which has been rarely observed and often confused with direct development from planula into ephyra. Planulae of Aurelia relicta Scorrano et al. 2017 and Cotylorhiza tuberculata (Macri 1778) settled and formed fully-grown polyps which transformed into ephyrae within several days. In distinction to monodisk strobilation, the basal polyp of indirect development was merely a non-tentaculate stalk that dissolved shortly after detachment of the ephyra. We provide a fully detailed description of this variant that increases reproductive plasticity within scyphozoan life cycles and is different than either true direct development or the monodisk strobilation. Our observations of this pattern in co-occurrence with mono- and polydisk strobilation in Aurelia spp. suggest that this reproductive mode may be crucial for the survival of some scyphozoan populations within the frame of a bet-hedging strategy and contribute to their long evolutionary success throughout the varied conditions of past and future oceans.

Ontogenetic changes in sensory gene expression in Bicyclus anynana butterflies

Animal behavior is largely driven by the information that animals are able to extract and process from their environment. However, the function and organization of sensory systems often change throughout ontogeny, particularly in animals that undergo indirect development. As an initial step toward investigating these ontogenetic changes at the molecular level, we characterized the sensory gene repertoire and examined the expression profiles of genes linked to vision and chemosensation in two life stages of an insect that undertakes a dramatic metamorphosis, the butterfly Bicyclus anynana. Using RNA-seq, we compared gene expression in the heads of late fifth instar larvae and newly-eclosed adults that were reared under identical conditions. Over 50% of all expressed genes were differentially expressed between the two developmental stages, with 4,046 genes upregulated in larval heads and 4,402 genes upregulated in adult heads. In larvae, upregulated vision-related genes were biased toward those involved with eye development, while phototransduction genes dominated the vision genes that were upregulated in adults. Moreover, the majority of the chemosensory genes we identified in the B. anynana genome were differentially expressed between larvae and adults, several of which share homology with genes linked to pheromone detection, host plant recognition, and foraging in other species of Lepidoptera. These results reveal promising candidates for furthering our understanding of sensory processing and behavior in the disparate developmental stages of butterflies and other animals that undergo metamorphosis.

Transcriptomic and proteomic dynamics during metamorphosis of Pacific oyster Crassostrea gigas

Many marine invertebrate phyla are characterized by indirect development. These animals transit from planktonic larvae to benthic adults via settlement and metamorphosis, which contributes to the adaption to the marine environment. Studying the biological process of metamorphosis is thus a key to understand the origin and evolution of indirect development. Numerous studies have been conducted on the relationships of metamorphosis with the marine environment, microorganisms, as well as the neurohormones, however, little is known on the gene regulation network (GRN) dynamics during metamorphosis. Metamorphosis competent pediveliger of Pacific oyster Crassostrea gigas was assayed in this study. By identifying genes enriched in competent pediveliger and early spat, as well as pediveligers treated with epinephrine, the dynamics of genes and proteins was examined with transcriptomics and proteomics methods. The results indicated significantly different gene regulation networks before, during, and post metamorphosis. Genes encoding membrane integrated receptors and related to the remodeling of the nervous system were upregulated before the initiation of metamorphosis. Massive biogenesis, e.g., various enzymes and structural proteins, occurred during metamorphosis. Correspondingly, the protein synthesis system was comprehensively activated after epinephrine stimulation. Hierarchical downstream gene networks were also stimulated, where some transcription factors showed different temporal response patterns, including some important Homeobox, basic helix-loop-helix factors and nuclear receptors. Nuclear receptors, as well as their retinoic acid receptor partners, should play critical roles during the oyster metamorphosis, although they may not be responsible for the initiation process. Enriched genes in early spat were mainly related to environmental stress responses, indicating the GRN complexity of the transition stage during oyster metamorphosis.

Conclusion

The chapter looks at what can be learnt and done using the model of development analysed in the book. It also examines the theoretical and practical implications of an approach such as Tostan’s for indirect development. Most importantly, this chapter details a theory of change that emerged from the analysis in the other chapters (motivation – deliberation – action). In addition, the chapter looks at other programmes, including Abriendo Oportunidades in Guatemala, SASA! In East Africa, and VAMP in India. Their models, field methods, and results are explored and compared with Tostan’s. This comparative analysis offers to the reader solid evidence of the results that indirect development programmes can achieve in various contexts and through various approaches. Finally, the chapter offers to the reader a look into the future, and how advocates for a rapid shift in development practices, calling for implementing genuine people-centred approaches.

Dynamics of Social Change: A Model for Indirect Development Practitioners

Chapter 7 explains why and how behavioural and social change happened. It investigates how in the HRE classes, participants contextualised the abstract human rights knowledge within their local understandings of the world and traditional values. That contextualisation fostered revisions in participants’ understanding of themselves and others and expanded individual and collective aspirations and capabilities. This chapter also analyses the role of the programme in creating a space where gender segregation could be overcome, where men and women could sit and talk together, sharing decisions, and how that affected the aspirations, perceived freedoms, and capabilities of the entire community. The theory described in chapter two is critically reviewed and expanded.

Human Rights Education in Action: The Programme Unfolds

Chapter 5 analyses in detail what happened during the HRE part of Tostan programme in the village. It analyses the different learning strategies used in class and show how they allowed participants to ground the abstract human rights knowledge into their concrete daily life. This chapter also gives an understanding of classroom dynamics and analyse how participants made sense of their experience in class. Chapter 5 might be particularly relevant for practitioners interested in implementing indirect development programmes through HRE, and to scholars studying what works in human development.

Introduction

Mainstream literature in international development has focussed either on advocating for ‘direct’ interventions (changing developing countries following western models) or on the dangers of intervention (for instance advocating for neoliberal trade as a solution to African poverty). Until recently, this dichotomy has obscured a possible third way, that of ‘indirect’ interventions, an approach that has gained increasing consensus in the last decade. While indirect development offers a solid approach, no models are analysed in the literature that can help scholars and practitioners advance this field further. This first chapter introduces the reader to the need for exploring models of indirect interventions and explains how each chapter contributes to grounding such a model on ethnographic evidence. This chapter also briefly provides the reader with critical information about research methodology and the characteristics of the ethnographic study, introducing Tostan communities as appropriate sites for a case study.

The early Cambrian fossil embryo Pseudooides is a direct-developing cnidarian, not an early ecdysozoan

Early Cambrian Pseudooides prima has been described from embryonic and post-embryonic stages of development, exhibiting long germ-band development. There has been some debate about the pattern of segmentation, but this interpretation, as among the earliest records of ecdysozoans, has been generally accepted. Here, we show that the ‘germ band’ of P. prima embryos separates along its mid axis during development, with the transverse furrows between the ‘somites’ unfolding into the polar aperture of the ten-sided theca of Hexaconularia sichuanensis , conventionally interpreted as a scyphozoan cnidarian; co-occurring post-embryonic remains of ecdysozoans are unrelated. We recognize H. sichuanensis as a junior synonym of P. prima as a consequence of identifying these two form-taxa as distinct developmental stages of the same organism. Direct development in P. prima parallels the co-occuring olivooids Olivooides, and Quadrapyrgites and Bayesian phylogenetic analysis of a novel phenotype dataset indicates that, despite differences in their tetra-, penta- and pseudo-hexa-radial symmetry, these hexangulaconulariids comprise a clade of scyphozoan medusozoans, with Arthrochites and conulariids, that all exhibit direct development from embryo to thecate polyp. The affinity of hexangulaconulariids and olivooids to extant scyphozoan medusozoans indicates that the prevalence of tetraradial symmetry and indirect development are a vestige of a broader spectrum of body-plan symmetries and developmental modes that was manifest in their early Phanerozoic counterparts.

Decoupled Maternal and Zygotic Genetic Effects Shape the Evolution of Development

Many animals develop indirectly via a larval stage that is morphologically and ecologically distinct from its adult form. Hundreds of lineages across animal phylogeny have secondarily lost larval forms, instead producing offspring that directly develop into adult form without a distinct larval ecological niche1–7. Indirect development in the sea is typically planktotrophic: females produce large numbers of small offspring that require exogenous planktonic food to develop before metamorphosing into benthic juveniles. Direct development is typically lecithotrophic: females produce a smaller number of larger eggs, each developing into a juvenile without the need for larval feeding, provisioned by yolk. Evolutionary theory suggests that these alternative developmental strategies represent stable alternative fitness peaks, while intermediate states are disfavored4,8–11. Transitions from planktotrophy to lecithotrophy thus require crossing a fitness valley and represent radical and coordinated transformations of life-history, fecundity, ecology, dispersal, and development7,12–16. Here we dissect this transition in Streblospio benedicti, the sole genetically tractable species that harbors both states as heritable variation17–19. We identify large-effect loci that act maternally to influence larval size and independent, unlinked large-effect loci that act zygotically to affect discrete aspects of larval morphology. Because lecithotrophs and planktotrophs differ in both size and morphology, the genetic basis of larval form exhibits strong maternal-by-zygotic epistasis for fitness20. The fitness of zygotic alleles depends on their maternal background, creating a positive frequency-dependence that may homogenize local populations. Developmental and population genetics interact to shape larval evolution.