Spatial and temporal dynamics of reproduction and settlement in the Pompeii worm Alvinella pompejana (Polychaeta: Alvinellidae)

Faure, Baptiste; Chevaldonné, Pierre; Pradillon, Florence; Thiébaut, Éric; Jollivet, Didier

doi:10.3354/meps07021

Cited by 16 publications

(23 citation statements)

References 33 publications

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“…2002; Copley et al. 2003; Faure et al. 2007) and have a very long history of evolution because their last speciation event (about 28 Ma for the most closely related and sibling species (see Chevaldonné et al.…”

Section: Discussionmentioning

confidence: 99%

Proteome evolution of deep-sea hydrothermal vent alvinellid polychaetes supports the ancestry of thermophily and subsequent adaptation to cold in some lineages

et al. 2017

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Temperature, perhaps more than any other environmental factor, is likely to influence the evolution of all organisms. It is also a very interesting factor to understand how genomes are shaped by selection over evolutionary timescales, as it potentially affects the whole genome. Among thermophilic prokaryotes, temperature affects both codon usage and protein composition to increase the stability of the transcriptional/translational machinery, and the resulting proteins need to be functional at high temperatures. Among eukaryotes less is known about genome evolution, and the tube-dwelling worms of the family Alvinellidae represent an excellent opportunity to test hypotheses about the emergence of thermophily in ectothermic metazoans. The Alvinellidae are a group of worms that experience varying thermal regimes, presumably having evolved into these niches over evolutionary times. Here we analyzed 423 putative orthologous loci derived from 6 alvinellid species including the thermophilic Alvinella pompejana and Paralvinella sulfincola. This comparative approach allowed us to assess amino acid composition, codon usage, divergence, direction of residue changes and the strength of selection along the alvinellid phylogeny, and to design a new eukaryotic thermophilic criterion based on significant differences in the residue composition of proteins. Contrary to expectations, the alvinellid ancestor of all present-day species seems to have been thermophilic, a trait subsequently maintained by purifying selection in lineages that still inhabit higher temperature environments. In contrast, lineages currently living in colder habitats likely evolved under selective relaxation, with some degree of positive selection for low-temperature adaptation at the protein level.

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Section: Discussionmentioning

confidence: 99%

Proteome evolution of deep-sea hydrothermal vent alvinellid polychaetes supports the ancestry of thermophily and subsequent adaptation to cold in some lineages

et al. 2017

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“…The larval development of this tube-dwelling worm is still largely unknown, but large yolk-rich eggs (150-200 μm), suggest that larval development is lecithotrophic and could be delayed in cold (1.5-2°C) water away from vent fields [ 12 ]. This worm species reproduces via internal fertilization and has nearly continuous gametogenesis, maximising its reproductive effort [ 17 ]. During mating, spermatozoids are transferred to the female in a spermatecae, and multiple paternity is possible [ 18 ].…”

Section: Introductionmentioning

confidence: 99%

Determining gene flow and the influence of selection across the equatorial barrier of the East Pacific Rise in the tube-dwelling polychaete Alvinella pompejana

et al. 2010

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BackgroundComparative phylogeography recently performed on the mitochondrial cytochrome oxidase I (mtCOI) gene from seven deep-sea vent species suggested that the East Pacific Rise fauna has undergone a vicariant event with the emergence of a north/south physical barrier at the Equator 1-2 Mya. Within this specialised fauna, the tube-dwelling polychaete Alvinella pompejana showed reciprocal monophyly at mtCOI on each side of the Equator (9°50'N/7°25'S), suggesting potential, ongoing allopatric speciation. However, the development of a barrier to gene flow is a long and complex process. Secondary contact between previously isolated populations can occur when physical isolation has not persisted long enough to result in reproductive isolation between genetically divergent lineages, potentially leading to hybridisation and subsequent allelic introgression. The present study evaluates the strength of the equatorial barrier to gene flow and tests for potential secondary contact zones between A. pompejana populations by comparing the mtCOI gene with nuclear genes.ResultsAllozyme frequencies and the analysis of nucleotide polymorphisms at three nuclear loci confirmed the north/south genetic differentiation of Alvinella pompejana populations along the East Pacific Rise. Migration was oriented north-to-south with a moderate allelic introgression between the two geographic groups over a narrow geographic range just south of the barrier. Multilocus analysis also indicated that southern populations have undergone demographic expansion as previously suggested by a multispecies approach. A strong shift in allozyme frequencies together with a high level of divergence between alleles and a low number of 'hybrid' individuals were observed between the northern and southern groups using the phosphoglucomutase gene. In contrast, the S-adenosylhomocysteine hydrolase gene exhibited reduced diversity and a lack of population differentiation possibly due to a selective sweep or hitch-hiking.ConclusionsThe equatorial barrier leading to the separation of East Pacific Rise vent fauna into two distinct geographic groups is still permeable to migration, with a probable north-to-south migration route for A. pompejana. This separation also coincides with demographic expansion in the southern East Pacific Rise. Our results suggest that allopatry resulting from ridge offsetting is a common mechanism of speciation for deep-sea hydrothermal vent organisms.

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“…As a consequence, colonists subjected to longer periods of high temperature (and associated hypoxia) may be maladapted to produce and use glycogen reserves and, thus, are not able to rapidly invest into reproduction. On the contrary, secondary settlers arriving in a much cooler state of the chimney and thus, more frequently exposed to colder oxygenated waters, are more likely to use their glycogen reserves to massively invest in the production of gametes as previously shown by Faure et al (2007). Colder conditions indeed seem to be a prerequisite for releasing fertilized eggs after pairing as embryos are not able to develop at temperatures greater than 15°C (Pradillon et al 2001).…”

Section: Selective Modalities For the Maintenance Of A Protected Polymentioning

confidence: 88%

“…Mature females collected during the 2002 and 2004 cruises were dissected before genotyping for allozymes (see Faure et al 2007 for more information about the female's oocytes counting procedure). For each female, coelomic fluid was carefully removed by making a ventral incision to the body wall of the trunk.…”

Section: Fecundity Determinationmentioning

confidence: 99%

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Balanced polymorphism at the Pgm-1 locus of the Pompeii worm Alvinella pompejana and its variant adaptability is only governed by two QE mutations at linked sites

Bioy¹,

Port²,

Sabourin³

et al. 2019

Preprint

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The polychaete Alvinella pompejana lives exclusively on the walls of deep-sea hydrothermal vents along the East Pacific Rise. This environment is considered as extreme and highly variable and the worm displays specific adaptations to withstand high temperature and hypoxia. Previous studies revealed the existence of a balanced polymorphism on the enzyme phosphoglucomutase associated with differences in the thermal habitat of the worm. Allozymes 90 and 100 exhibited different optimal enzyme activities and thermostabilities.The exploration of the mutational landscape for allozyme variation of the phosphoglucomutase1 revealed the maintenance of four highly divergent allelic lineages that encode the three most frequent electromorphs, these alleles occurring at different frequencies in populations over the worm's geographic range. Enzyme polymorphism is only governed by two linked amino-acid replacements located in exon 3 (E155Q and E190Q). Unlike other studies dealing with the non-synonymous variations of the Pgm genes, these substitutions are not linked to other cryptic amino-acid polymorphisms. Overdominance under specific environmental 'hot' conditions should represent the most likely way for the long-term persistence of these isoforms. Using directed mutagenesis, overexpression of the three recombinant variants allowed us to test the additive effect of these two mutations on the biochemical properties of this enzyme. Results are coherent with those previously obtained from native proteins and reveal a thermodynamic trade-off between the protein thermostability and catalysis, which is likely to explain the long-term selection of these functional phenotypes before their geographic separation across the Equator with the emergence of a barrier to dispersal, about 1.2 Mya.

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Spatial and temporal dynamics of reproduction and settlement in the Pompeii worm Alvinella pompejana (Polychaeta: Alvinellidae)

Cited by 16 publications

References 33 publications

Proteome evolution of deep-sea hydrothermal vent alvinellid polychaetes supports the ancestry of thermophily and subsequent adaptation to cold in some lineages

Proteome evolution of deep-sea hydrothermal vent alvinellid polychaetes supports the ancestry of thermophily and subsequent adaptation to cold in some lineages

Determining gene flow and the influence of selection across the equatorial barrier of the East Pacific Rise in the tube-dwelling polychaete Alvinella pompejana

Balanced polymorphism at the Pgm-1 locus of the Pompeii worm Alvinella pompejana and its variant adaptability is only governed by two QE mutations at linked sites

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