The evolution of the Metazoa is among the greatest success stories in Earth history. From modest origins, probably in the Cryogenian (~720 - 635 Ma), metazoans had acquired hard parts, and a vast range of life strategies and body plans by the middle Cambrian (around 520 Ma). This leaves a long delay between the origin of the Metazoa and their rise to ecological dominance. A popular explanatory hypothesis for this delay is that atmospheric oxygen levels, low in the Proterozoic (< 0.001 % PAL), began to rise towards modern levels towards the end of the Neoproterozoic. Among the earliest known putative metazoans are Namacalathus, Namapoikia and Cloudina, calcified marine invertebrates abundant in the latest Ediacaran (~ 548-541 Ma) Nama Group, Namibia. Although they were pioneers of metazoan biomineralisation, little is known of their affinities or palaeocology. The Nama Group, a well-characterised, relatively undeformed mixed carbonate and siliciclastic succession, provides a rare opportunity to investigate the palaeoecology of these important organisms in their environmental context. New geochemical data from the Nama Group confirm the heterogeneity of Ediacaran redox conditions. These contextualise in situ fossil assemblages which reveal diverse ecological strategies among the calcified metazoans of the Nama Group, and offer constraints on their affinities. Based on its large size (< 1 m), modular body plan and internal structure of interlinked tubules, Namapoikia was a long-lived specialist and possible Poriferan. I show that Namapoikia colonised both lithified and living microbial substrates in oxic, mid-ramp reef crypts. By contrast, size and occurrence data show that Namacalathus was an environmental generalist, forming large, thick aggregations in persistently oxic, mid-ramp reef environments but opportunistically exploiting the transiently oxic, inner ramp setting. Bilaterally symmetrical, asexual budding and a microlamellar skeletal ultrastructure suggest that Namacalathus may have been an early lophophorate, and had flexible growth depending on environmental setting, showing a cup diameter of 2 – 35 mm, and size distributions varying with substrate type, redox and water depth. In oxic mid-ramp reefs, Cloudina constructed large (> 20 m) reefs showing mutual attachment and consistent orientation in life position, making it the earliest known reef-building metazoan and suggesting that it was a passive suspension feeder. I further present food webs based on fossil assemblages from Ediacaran to Cambrian Stage 4 carbonate successions and evaluate their usefulness in tracking metazoan trophic diversification in the early Cambrian. Ediacaran redox conditions were a major control on the ecologies of the earliest metazoans. A requirement for oxygen made persistently oxic conditions a prerequisite for complex and long-lived ecologies, while highly flexible life strategies were used to exploit changeable environments. Ediacaran metazoans represent a phylogenetic and ecological foreshadowing of the complexity of the Phanerozoic, but it was not until much later that the Metazoa would attain their evolutionary potential.

La signalisation stéroïdienne médiée par des récepteurs nucléaires est impliquée dans de nombreux processus ayant trait au développement des animaux. La compréhension de ces phénomènes est importante pour répondre à des questions de santé publique, d’agronomie ou de biologie de la conservation. Ceci nécessite de connaître et de mettre en relation l’évolution des récepteurs qui fixent ces stéroïdes et des voies de synthèse qui produisent les stéroïdes. Mon travail s’est articulé autour de trois grands axes. 1. La mise à jour des relations de parenté entre les récepteurs nucléaires impliqués dans la fixation des stéroïdes, mais aussi de ceux qui sont impliqués dans la régulation de la stéroïdogenèse, pour comprendre quand et dans quel contexte cette machinerie est apparue. 2. La démonstration que les enzymes impliquées dans la stéroïdogenèse étaient apparues indépendamment par recrutement d’enzymes à spécificité de substrat plus large impliquées dans la détoxification des xénobiotiques. 3. L'élucidation des relations de parenté entre des voies métaboliques, montrant que les voies de la stéroïdogenèse avaient évolué comme des voies de dégradation du cholestérol. Ces résultats aboutissent à un modèle dans lequel la signalisation hormonale des animaux à symétrie bilatérale serait l’héritière de voies de détoxification de molécules stéroïdiennes contenues dans leur alimentation. Ce modèle expliquerait le couplage entre l’accumulation de nutriments et la maturation sexuelle, ainsi que les nombreux dérèglements touchant à la fois le métabolisme et la reproduction dus aux perturbateurs endocriniens ou à certaines molécules thérapeutiques. / Nuclear receptor mediated steroid signaling is involved in many processes in metazoandevelopment, such as puberty in vertebrates, molting in insects and entry into infective stage in some parasitic nematodes. Understanding those phenomena is important regarding public health, agronomical and conservation biology issues. This necessitates to know and to explore the interactions between the evolution of steroid-binding receptors and steroid-synthesizing pathways. My work was articulated around three major parts. First, using the historical expertise of the laboratory, I updated the relationships between nuclear receptors that are involved in steroid binding, but also from all those that are involved in steroidogenesis regulation, in order to elucidate when and in which context this machinery has arisen. Second, using a classical comparative genomic approach, I showed that the steroidogenetic enzymes have appeared independently by duplication from xenobiotic-metabolizing enzyme with a wider range of substrate specificity.Third, I explored the relationships between metabolic pathways using tools from comparative anatomy. This has confirmed and completed the previous results, showing that steroidogenetic pathways have evolved with the pattern of cholesterol degradation pathways.The synthesis of all these results has led to an evolutionary model where hormonal signaling in bilaterian animals has been inherited from the detoxification of dietary sterols. This model may explain the coupling between nutrient accumulation and sexual maturation, and also the link between metabolic disorders and endocrine disruption due to environmental chemicals or drugs.

The main aim of this thesis was to determine how marine metazoans might persist as ocean acidification (OA) conditions intensify. This was done using a combination of field surveys, field transplants and laboratory experiments with polychaetes from a site where volcanically-derived CO2 gas bubbles through the seafloor and drives the seawater pH down, resulting in a marine ecosystem representative of global OA projections for, or before, the year 2100. My first objective was to identify phenotypes, or traits, associated with OA tolerance (Chapter 2 and 5). To do this, I characterized the distribution of dominant calcifying polychaetes along natural pH gradients and used a comparative species recruitment trial to investigate life history traits underlying species’ OA tolerance, or vulnerability. I first found two dominant, closely related species of polychaete: Pileolaria militaris Claparède, 1870 and Simplaria sp. (Serpulidae, Spirorbinae). I then found that increased fecundity and rapid settlement are important traits in determining species’ abilities to persist in low pH environments (Chapter 2). Afterwhich, I investigated the life history traits of the non-calcifying polychaete, Platynereis dumerilii (Audouin & Milne Edwards, 1834), of one of the few species from the low pH site known to have broadcasting, pelagic development. I performed breeding experiments on P. dumerilii collected in both ambient and low pH sites and found that specimens from the low pH site were actually the direct developing brooder sister species, Platynereis massiliensis (Moquin-Tandon, 1869). By reanalayzing the distributions of both species at each site using genetic barcoding, I found clear evidence that direct development and brooding are dominant traits at low pH site, and for OA persistence (Chapter 5). My second objective was to use reciprocal transplant experiments to compare the relative importance of local adaptation and/or plasticity as potential mechanisms responsible for the differential tolerances of populations of the polychaete species Simplaria sp. to low pH. Laboratory transplants indicate that a local adaptation response occurred through genetic accommodation in the Simplaria sp. population from the low pH site. However, neither local adaptation nor plasticity appeared responsible for this species natural low pH persistence when assessed in situ (Chapter 3 & 4). My final objective was to create a framework using the polychaete vent model to identify other types of marine metazoans that are likely to be able to adapt to, and survive, under the predicted environmental conditions (Chapter 5). I overviewed the life history strategies of all dominant polychaetes in the low pH sites, and related trends in their life history strategies to those of other marine invertebrates. Brooding and direct development appear to be key traits for species likely to persist in future oceans pH. I conclude by summarizing how research regarding evolutionary responses may be advanced to add confidence to our projections of future marine metazoan responses.

Exon shuffling foi primeiramente proposto por Walter Gilbert em 1978 como um mecanismo em que exons de diferentes genes podem ser combinados, levando à formação de novos genes. O mecanismo de exon shuffling é favorecido por recombinações intrônicas e está correlacionado com a simetria de exons. Evidências deste mecanismo provém de análises de combinações de fases de introns, correlações entre bordas de exons e de domínios protéicos e da recorrência de domínios em diversas proteínas. Dessa forma, a evolução de proteínas formadas por exon shuffling pode ser inferida considerando a organização exon-intron dos genes, o padrão de combinações de fases de introns e a organização de domínios nas proteínas. Neste sentido, regiões protéicas que possivelmente foram originadas por eventos de exon shuffling foram identificadas através de análises em larga escala em diferentes espécies eucarióticas. A estratégia foi baseada no alinhamento entre todas as proteínas anotadas de uma determinada espécie e a verificação da presença de introns e suas respectivas fases em torno das regiões alinhadas. Nós verificamos que eventos de exon shuffling em eucariotos antigos, de origem anterior aos Metazoa, são predominantemente simétricos 0-0, enquanto nos metazoários a predominância é de unidades simétricas 1-1. Esses dados confirmam idéias anteriores de que a transição para a multicelularidade animal foi marcada pelo embaralhamento extensivo de exons e domínios 1-1. O metazoário basal Trichoplax adhaerens pode ser considerado um representante desta transição, evidenciada pelas freqüências balanceadas de regiões simétricas 0-0 e 1-1. O sinal de flanqueamento por introns em torno das bordas de domínios protéicos confirmou os resultados obtidos através dos alinhamentos, com a prevalência de domínios 0-0 em não metazoários e 1-1 em metazaoários. Um agrupamento hierárquico de domínios flanqueados por introns foi construído, permitindo identificar domínios ou grupos de domínios com evidência de expansões em períodos específicos, como nos vertebrados. Por fim, os genes envolvidos em eventos de exon shuffling foram analisados quanto ao enriquecimento em termos do Gene Ontology. Os resultados indicaram que este mecanismo contribuiu significativamente para a formação de genes relacionados com uma grande diversidade de termos, alguns dos quais envolvidos diretamente com características de metazoários e vertebrados, tais como matriz extracelular, adesão, coagulação sangüínea, processos do sistema imune e sistema nervoso / Exon shuffling was first proposed by Walter Gilbert in 1979 as a mechanism in which exons from different genes could be combined to lead the creation of new genes. The mechanism of exon shuffling is favored by intronic recombinations and it is correlated with symmetry of exons. Evidence of this mechanism come from analyses of intron phase combinations, correlations between the borders of exons and domains and domain recurrence in several proteins. Taking this into account, the evolution of proteins formed by exon shuffling can be inferred regarding the exonintron organization of the genes, the pattern of intron phase combinations and the protein domain organization. In this sense, protein regions that were probably arose by exon shuffling events were identified through a large scale analysis in several eukaryotic species. The strategy was based on alignments between all annotated proteins from a given species. Then, the aligned regions were verified in respect with intron phase combinations surrounding them. We have found that exon shuffling events in early eukaryotes are preferentially symmetric of phase 0, while in metazoans, the preference is for 1-1 symmetric units. These data confirms previous ideas that the transition to animal multicellularity was marked by extensive 1-1 exon shuffling. The basal metazoan Trichoplax adhaerens is a representative of this transition, evidenced by the balanced frequencies of 0-0 and 1-1 symmetric regions. The signal of intron flanking around the borders of protein domains corroborated previous analyses, showing that non metazoans have higher frequencies of 0-0 domains and metazoans have higher frequencies of 1-1 domains. A hierarchical clustering of domains flanked by introns was built, allowing us to identify domains or groups of domains with evidence of expansions during specific periods, such as in vertebrates. Finally, genes involved in exon shuffling events were analyzed regarding the Gene Ontology enriched terms. The results indicated that this mechanism significantly contributed to the creation of genes related with a large diversity of terms, some of them are directly involved with features of metazoans and vertebrates, such as extracellular matrix, cell adhesion, blood coagulation and immune and nervous system processes

Exon shuffling foi primeiramente proposto por Walter Gilbert em 1978 como um mecanismo em que exons de diferentes genes podem ser combinados, levando à formação de novos genes. O mecanismo de exon shuffling é favorecido por recombinações intrônicas e está correlacionado com a simetria de exons. Evidências deste mecanismo provém de análises de combinações de fases de introns, correlações entre bordas de exons e de domínios protéicos e da recorrência de domínios em diversas proteínas. Dessa forma, a evolução de proteínas formadas por exon shuffling pode ser inferida considerando a organização exon-intron dos genes, o padrão de combinações de fases de introns e a organização de domínios nas proteínas. Neste sentido, regiões protéicas que possivelmente foram originadas por eventos de exon shuffling foram identificadas através de análises em larga escala em diferentes espécies eucarióticas. A estratégia foi baseada no alinhamento entre todas as proteínas anotadas de uma determinada espécie e a verificação da presença de introns e suas respectivas fases em torno das regiões alinhadas. Nós verificamos que eventos de exon shuffling em eucariotos antigos, de origem anterior aos Metazoa, são predominantemente simétricos 0-0, enquanto nos metazoários a predominância é de unidades simétricas 1-1. Esses dados confirmam idéias anteriores de que a transição para a multicelularidade animal foi marcada pelo embaralhamento extensivo de exons e domínios 1-1. O metazoário basal Trichoplax adhaerens pode ser considerado um representante desta transição, evidenciada pelas freqüências balanceadas de regiões simétricas 0-0 e 1-1. O sinal de flanqueamento por introns em torno das bordas de domínios protéicos confirmou os resultados obtidos através dos alinhamentos, com a prevalência de domínios 0-0 em não metazoários e 1-1 em metazaoários. Um agrupamento hierárquico de domínios flanqueados por introns foi construído, permitindo identificar domínios ou grupos de domínios com evidência de expansões em períodos específicos, como nos vertebrados. Por fim, os genes envolvidos em eventos de exon shuffling foram analisados quanto ao enriquecimento em termos do Gene Ontology. Os resultados indicaram que este mecanismo contribuiu significativamente para a formação de genes relacionados com uma grande diversidade de termos, alguns dos quais envolvidos diretamente com características de metazoários e vertebrados, tais como matriz extracelular, adesão, coagulação sangüínea, processos do sistema imune e sistema nervoso / Exon shuffling was first proposed by Walter Gilbert in 1979 as a mechanism in which exons from different genes could be combined to lead the creation of new genes. The mechanism of exon shuffling is favored by intronic recombinations and it is correlated with symmetry of exons. Evidence of this mechanism come from analyses of intron phase combinations, correlations between the borders of exons and domains and domain recurrence in several proteins. Taking this into account, the evolution of proteins formed by exon shuffling can be inferred regarding the exonintron organization of the genes, the pattern of intron phase combinations and the protein domain organization. In this sense, protein regions that were probably arose by exon shuffling events were identified through a large scale analysis in several eukaryotic species. The strategy was based on alignments between all annotated proteins from a given species. Then, the aligned regions were verified in respect with intron phase combinations surrounding them. We have found that exon shuffling events in early eukaryotes are preferentially symmetric of phase 0, while in metazoans, the preference is for 1-1 symmetric units. These data confirms previous ideas that the transition to animal multicellularity was marked by extensive 1-1 exon shuffling. The basal metazoan Trichoplax adhaerens is a representative of this transition, evidenced by the balanced frequencies of 0-0 and 1-1 symmetric regions. The signal of intron flanking around the borders of protein domains corroborated previous analyses, showing that non metazoans have higher frequencies of 0-0 domains and metazoans have higher frequencies of 1-1 domains. A hierarchical clustering of domains flanked by introns was built, allowing us to identify domains or groups of domains with evidence of expansions during specific periods, such as in vertebrates. Finally, genes involved in exon shuffling events were analyzed regarding the Gene Ontology enriched terms. The results indicated that this mechanism significantly contributed to the creation of genes related with a large diversity of terms, some of them are directly involved with features of metazoans and vertebrates, such as extracellular matrix, cell adhesion, blood coagulation and immune and nervous system processes

La métamorphose est une étape cruciale du cycle de vie de beaucoup de métazoaires. Elle est définie comme la transition d’une larve en un juvénile, souvent accompagnée de changements drastiques de morphologie, physiologie et de niche écologique. Le rôle des hormones thyroïdiennes a été mis en évidence dans la métamorphose des amphibiens, mais aussi de nombreux autres chordés comme certains poissons téléostéens ou l'amphioxus, suggérant que ce système était déjà présent et impliqué dans la métamorphose chez l'ancêtre commun de tous les chordés.Nous avons étudié le lien entre hormones thyroïdiennes et métamorphose selon deux axes. Premièrement, nous avons étudié la coordination entre la métamorphose et le recrutement larvaire, chez le chirurgien bagnard Acanthurus triostegus. Ce travail nous a permis de mieux comprendre le rôle de l’hormone thyroïdienne comme signal déclencheur d'une transition écologique importante. Dans le second axe de travail nous avons examiné l’origine de la signalisation thyroïdienne. Chez l’annélide Platynereis dumerili, nous avons identifié un récepteur fonctionnel des hormones et un rôle de l’hormone thyroïdienne dans son développement. Cela qui nous permet de démontrer que la signalisation thyroïdienne était présente à l’origine des bilateriens. Nous avons également mis en évidence un rôle des hormones thyroïdiennes dans le développement de cette espèce. Enfin dans le troisième axe nous nous sommes penchés sur l’origine de la synthèse de l’hormone thyroïdienne en retraçant l’évolution de la thyroglobuline, la protéine nécessaire à la production d’hormone chez les vertébrés. Son absence dans les autres taxons, alors que les dérivés de l’hormone y ont un rôle biologique, pose la question des mécanismes ancestraux de synthèse de ces hormones.Ces travaux explorent l’évolution de la signalisation thyroïdienne et proposent d’aborder la question du lien avec la métamorphose d’un point de vue évolutif et non-seulement développemental, afin de mieux comprendre la diversité des métamorphoses observées dans le monde animal. / Metamorphosis is a critical life step of many metazoans. It is defined as the transition between a larva and a juvenile. It comes with major changes of morphology, physiology and ecology. The role of thyroid hormone has been proven in the metamorphosis of amphibians but also in many other chordates such as teleost fishes or the amphioxus. This suggests that this system was functional and involved in the metamorphosis of the common ancestor of all chordates.We studied the link between thyroid hormones and metamorphosis according to two axes. First, we studied the coordination between metamorphosis and the larval colonization, using the convicted surgeon fish Acanthurus triostegus as a model. This work allowed us to better understand the role of thyroid hormones as a trigger signal of a major ecological transition. On the second axis, we investigated the origin of thyroid hormone signalization. In the annelid Platynereis dumerilii, we identified a functional thyroid hormone receptor and a role of TH in its development. This proves that thyroid hormone signaling was present at the basis of bilaterians. We also assessed the question of the origin of thyroid hormone synthesis by tracing back the evolution of the thyroglobulin, the protein mandatory for thyroid hormone synthesis in vertebrates. It absence in the other taxa, whereas thyroid hormone derivatives have a biological role, asks the question of the ancestral mechanisms of thyroid hormone synthesis.These works investigate the evolution of the thyroid hormone signalization and suggest to tackle the question of the link with metamorphosis from an evolutionary perspective, and not only from a developmental one, in order to better understand the diversity of metamorphosis overserved in the animal kingdom.