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Pradillon, F.

Publications and source records attributed to Pradillon, F..

6 recordsLinked to original sources

Genetic sex determination in three closely related hydrothermal vent gastropods, one of which has intersex individuals

Molluscs have a wide variety of sexual systems and have undergone many transitions from separate sexes to hermaphroditism or vice versa, which is of interest for studying the evolution of sex determination and differentiation. Following the serendipitous observation that sex was the primary driver of genetic structure in the hydrothermal vent gastropod Alviniconcha boucheti, we investigated sexual systems and sex determination in this species and two others of the same genus. We combined genome-wide multi-locus genotypes obtained from RAD sequencing with anatomical observations of the gonads of the three Alviniconcha species occurring in the southwest Pacific Ocean: A. boucheti (n=199), A. strummeri (n=41 ind.) and A. kojimai (n=246). In two of the species (A. boucheti and A. strummeri), the sexes are separate and genetically determined by a male-heterogametic (XY) system. External observation of the gonads in the third species (A. kojimai) also suggested that the sexes were separate, but histological analyses revealed that 76% of the individuals classified as females from external observation of the gonads presented a mosaic of male and female reproductive tissue. Empirical analyses and simulations showed nonetheless that 14 RAD loci were sex-linked with an XY signature in A. kojimai (as compared with 64 in A. strummeri and 373 in A. boucheti). Comparison across species and mapping of RAD loci to a non-contiguous reference genome assembly of the related species A. marisindica showed that all sex-linked loci identified in A. kojimai are located on five scaffolds that also contain 15 and 67 sex-linked RAD loci in the other two species, respectively. These results suggest that all three Alviniconcha species share the same XY sex determination system, but that the gonad of XX A. kojimai individuals are invaded by a variable proportion of male reproductive tissue. It remains to be seen whether the male tissue in these intersex individuals is functional or not. The identification of Y-specific RAD loci (found only in A. boucheti) and the phylogenetic analysis of three sex-linked loci shared by all species suggested that X-Y recombination has evolved differently within each species. This situation of three species showing variation in gonadal development around a probably common sex determination system provides new insights into the reproductive mode of poorly known deep-sea species and questions the evolution of gametogenetic polymorphism in these species.

evolutionary biology↗

Symbioses of alvinocaridid shrimps from the South West Pacific: No chemosymbiotic diets but partially conserved gut microbiomes

Rimicaris exoculata shrimps from hydrothermal vent ecosystems are known to host dense epibiotic communities inside their enlarged heads and digestive systems. Conversely, other shrimps from the family, described as opportunistic feeders have received less attention. We examined the nutrition and bacterial communities colonizing "head" chambers and digestive systems of three other alvinocaridids - Rimicaris variabilis, Nautilocaris saintlaurentae and Manuscaris sp. - using a combination of electron microscopy, stable isotopes and sequencing approaches. Our observations inside "head" cavities and on mouthparts showed only a really low coverage of bacterial epibionts. In addition, no clear correlation between isotopic ratios and relative abundance of epibionts on mouthparts could be established among shrimp individuals. Altogether, these results suggest that none of these alvinocaridids rely on chemosynthetic epibionts as their main source of nutrition. Our analyses also revealed a substantial presence of several Firmicutes within the foreguts and midguts of these shrimps, which closest known lineages were systematically digestive epibionts associated with alvinocaridids, and more broadly from digestive systems of other crustaceans from marine and terrestrial ecosystems. Overall, our study opens new perspectives not only about chemosynthetic symbioses of vent shrimps, but more largely about digestive microbiomes with potential ancient and evolutionarily conserved bacterial partnerships among crustaceans.

evolutionary biology↗

Anatomy and Symbiosis of the digestive system of the vent shrimps Rimicaris exoculata and Rimicaris chacei revealed through imaging approaches.

The shrimps Rimicaris exoculata and Rimicaris chacei are visually dominant fauna co-occurring at deep-sea hydrothermal sites of the Mid-Atlantic Ridge (MAR). Their co-existence was related to contrasted life-history traits, among which differences in their diet and reliance on chemoautotrophic symbionts at adult stage. Both shrimps are colonized by diversified chemosynthetic symbiotic microbial communities in their cephalothoracic cavity. Symbiotic association with bacteria was also evidenced in their digestive system, and the major lineages were identified through sequencing (Mycoplasmatales lineages mainly in the foregut and Deferribacteres lineages mainly in the midgut) but their clear distribution within each host species was not assessed. For the first time, we used Fluorescence in situ Hybridization (FISH) to visualize these lineages. Then, we described their association with digestive structures of both Rimicaris species. The aim was to identify possible differences between host species that could be related to their different life-history traits. For this purpose, we first developed specific FISH probes targeting Deferribacteres and Mycoplasmatales lineages identified in the digestive system of these shrimps. After signal specificity validation for each the new probe, we showed a partitioning of the bacterial lineages according to the digestive organ. Despite morphological differences between the foregut of R. exoculata and R. chacei that could be related to the adult diet, our FISH results showed overall similar distribution of digestive symbionts for the two host species. However, a more comprehensive study is needed with specimens at different life or molt stages to bring potentially host specific patterns out. Such comparative approach using FISH is now warranted thanks to our newly designed probes. These will be valuable tools to track symbiont lineages in the environment, allowing a better understanding of their relationship with their host along its life cycle, including acquisition mechanisms.

microbiology↗

Reproductive strategies in vent shrimps shaped by feeding ecology with intriguing seasonality unlinked to surface productivity

Variations in offspring production according to feeding strategies or food supply have been recognized in many animals from various ecosystems. Despite an unusual trophic structure based on non-photosynthetic primary production, these relationships remain largely under-studied in chemosynthetic ecosystems. Here, we use Rimicaris shrimps from deep-sea hydrothermal vents as a study case to explore relations between reproduction, diets and food supply in these environments. For that, we compared reproductive outputs of three congeneric shrimps differing by their diets. They inhabit vents located under oligotrophic waters of tropical gyres with opposed latitudes, allowing us to also examine the prevalence of phylogenetic vs environmental drivers in their reproductive rhythms. For this we used both our original data and a compilation of published observations on the presence of ovigerous females covering various seasons over the past 35 years. We report distinct egg production trends between Rimicaris species relying solely on chemosymbiosis - R. exoculata and R. kairei - and those relying on mixotrophy - R. chacei - where R. chacei produces broods with higher numbers of smaller eggs. Besides, our data and historical records suggest a reproductive period with substantial proportions of brooding females mostly between January and early April for all examined species whatever the region. Intriguingly, this periodicity does not correspond to seasonal variations in surface production with presence of brooding females during either boreal winter or austral summer. These observations contrast with the long-standing paradigm in deep-sea species for which periodic reproductive patterns have always been attributed to seasonal variations of photosynthetic production sinking from surface. Our results suggest the presence of intrinsic basis for biological rhythms in the deep sea, and bring to light the importance of having year-round observations in order to understand life history of vent animals.

ecology↗

Population structure and reproduction of the alvinocaridid shrimp Rimicaris exoculata on the Mid-Atlantic Ridge: variations between habitats and vent fields

Rimicaris exoculata is a dominant species of deep Mid-Atlantic Ridge (MAR) vent fields and inhabits areas close to vent emissions at depths below 2000 m. Its high abundance and strong genetic connectivity along the MAR point at a remarkable ability to produce dispersing larval stages. However, the reproduction of this species long remained enigmatic because brooding females were rarely observed. Here, we describe the population structure and reproduction of R. exoculata at the Snake Pit and TAG vent fields (3600m depth) for the months of January-February. We observed major differences in population structure between habitats within a single vent field: females widely dominate the large swarms near active venting while inactive peripheries are inhabited by large males. Low temperature diffusion zones are mainly colonized by small juveniles of R. chacei instead of R. exoculata. Size structure of populations from dense active areas is polymodal at both fields, suggesting discontinuous recruitment. Male and female sizes did not vary across habitats and vent fields, with sexually mature female being slightly larger than males. In contrast to previous studies, hundreds of ovigerous females were observed at both vent fields, suggesting seasonal reproduction. Proportion of ovigerous females among sexually mature females were similar between vent fields (36.7 %). However, reproductive output was lower at TAG, where ovigerous females had smaller size-specific fecundity and egg size, and more aborted broods. Broods were colonized by the dirivultid copepod Stygiopontius pectinatus at both vent fields, apparently without deleterious effect on egg development. In the light of the observed variability in R. exoculata population structure, we propose a hypothetical scenario depicting its mating system and brooding behavior, and discuss more generally intraspecific interactions during its benthic life stages.

ecology↗

Population structure and environmental niches of Rimicaris shrimps from the Mid Atlantic Ridge

Among the endemic and specialized fauna from hydrothermal vents, Rimicaris shrimp surely constitutes one of the most important and emblematic components of these ecosystems. In the Mid Atlantic Ridge, two species affiliated to this genus co-occur: Rimicaris exoculata and Rimicaris chacei that differ by their morphology, their trophic regime as well as by their abundance. The first forms large and dense aggregations on active vent chimney walls in close proximity to vent fluid emissions, whereas the second is recognized as much less conspicuous, living mostly in scattered groups or solitary further away from the fluids. However, the recent revision of Rimicaris juvenile stages from the Mid Atlantic Ridge shows that R. chacei abundance would be higher than expected at these early life stages. Here, we describe and compare the population structures of R. exoculata and R. chacei at the Snake Pit and TAG vent fields. We show distinct population demographics between the two co-occurring shrimps with a large post settlement collapse in R. chacei population suggesting a large juvenile mortality for this species. We also observe important spatial segregation patterns between the two species and their different life stages. Additionally, our results highlight distinct niches for the earliest juvenile stages of both R. exoculata and R. chacei, compared to all the other life stages. Finally, we discuss the potential factors - predation and competitive interactions among others - that could explain the differences we observe in the population structure of these two species.

ecology↗