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Classical and computed tomographic anatomical analyses in a not-so-cryptic Alviniconcha species complex from hydrothermal vents in the SW Pacific.

ABSTRACT: The chemosymbiotic gastropod Alviniconcha (Provannidae), first described in 1988, is one of the most emblematic hydrothermal-vent taxa described from the Central Indian Ridge and the Southwest (SW) Pacific. Symbiotic bacteria found in the gill of Alviniconcha are thought to be their principal source of nutrition. In the SW Pacific, species distributions for A. kojimai, A. boucheti - and to a lesser extent A. strummeri - overlap. While Alviniconcha species do not appear to truly co-exist in these highly energetic but spatially limited habitats, certain species regularly co-occur within a single vent field and in rare instances, the same edifice. Past research suggests that SW-Pacific Alviniconcha species might aggregate around fluids with distinct geothermal profiles. These small-scale distribution patterns have been attributed to differences in their symbiont assemblages or host physiologies. However, little is known about the anatomy of most Alviniconcha species, beyond that detailed for the type species Alviniconcha hessleri, whose geographic range does not overlap with other congeners. In fact, species within this genus are currently described as cryptic, despite the absence of any comparative morphological studies to assess this. To test whether the genus is genuinely cryptic and identify any functional differences in host anatomy that might also mediate habitat partitioning in SW Pacific species, the current study examined the morphoanatomy of A. kojimai, A. boucheti and A. strummeri from the Fatu Kapa vent field, an area of hydrothermal activity recently discovered north of the Lau Basin near the Wallis and Futuna Islands and the only known example where all three species occur within adjacent vent fields. A combination of detailed dissections, histology and X-ray computed tomography demonstrate that A. kojimai, A. strummeri and A. boucheti are readily identifiable based on shell morphology and ornamentation alone, and therefore not truly cryptic. These traits provide a rapid and reliable means for species identification. However, aside from some subtle differences in radular morphology, these species of Alviniconcha exhibit conserved anatomical features, providing no evidence that functional host anatomy is implicated in habitat partitioning. This provides support for the current belief that host-species distributions are probably governed by symbiont-mediated physiological factors.

SUBMITTER: Laming SR

PROVIDER: S-EPMC7203863 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Classical and computed tomographic anatomical analyses in a not-so-cryptic Alviniconcha species complex from hydrothermal vents in the SW Pacific.

Laming Sven R SR Hourdez Stéphane S Cambon-Bonavita Marie-Anne MA Pradillon Florence F

Frontiers in zoology 20200507

The chemosymbiotic gastropod Alviniconcha (Provannidae), first described in 1988, is one of the most emblematic hydrothermal-vent taxa described from the Central Indian Ridge and the Southwest (SW) Pacific. Symbiotic bacteria found in the gill of Alviniconcha are thought to be their principal source of nutrition. In the SW Pacific, species distributions for A. kojimai, A. boucheti - and to a lesser extent A. strummeri - overlap. While Alviniconcha specie ...[more]

PMID: 32391066

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Project description:BackgroundThe inhabitants of deep-sea hydrothermal vents occupy ephemeral island-like habitats distributed sporadically along tectonic spreading-centers, back-arc basins, and volcanically active seamounts. The majority of vent taxa undergo a pelagic larval phase, and thus varying degrees of geographical subdivision, ranging from no impedance of dispersal to complete isolation, often exist among taxa that span common geomorphological boundaries. Two lineages of Bathymodiolus mussels segregate on either side of the Easter Microplate, a boundary that separates the East Pacific Rise from spreading centers connected to the Pacific-Antarctic Ridge.ResultsA recent sample from the northwest flank of the Easter Microplate contained an admixture of northern and southern mitochondrial haplotypes and corresponding alleles at five nuclear gene loci. Genotypic frequencies in this sample did not fit random mating expectation. Significant heterozygote deficiencies at nuclear loci and gametic disequilibria between loci suggested that this transitional region might be a 'Tension Zone' maintained by immigration of parental types and possibly hybrid unfitness. An analysis of recombination history in the nuclear genes suggests a prolonged history of parapatric contact between the two mussel lineages. We hereby elevate the southern lineage to species status as Bathymodiolus antarcticus n. sp. and restrict the use of Bathymodiolus thermophilus to the northern lineage.ConclusionsBecause B. thermophilus s.s. exhibits no evidence for subdivision or isolation-by-distance across its 4000 km range along the EPR axis and Galápagos Rift, partial isolation of B. antarcticus n. sp. requires explanation. The time needed to produce the observed degree of mitochondrial differentiation is consistent with the age of the Easter Microplate (2.5 to 5.3 million years). The complex geomorphology of the Easter Microplate region forces strong cross-axis currents that might disrupt self-recruitment of mussels by removing planktotrophic larvae from the ridge axis. Furthermore, frequent local extinction events in this tectonically dynamic region might produce a demographic sink rather than a source for dispersing mussel larvae. Historical changes in tectonic rates and current patterns appear to permit intermittent contact and introgression between the two species.

Project description:BackgroundChemolithoautotrophic primary production sustains dense invertebrate communities at deep-sea hydrothermal vents and hydrocarbon seeps. Symbiotic bacteria that oxidize dissolved sulfur, methane, and hydrogen gases nourish bathymodiolin mussels that thrive in these environments worldwide. The mussel symbionts are newly acquired in each generation via infection by free-living forms. This study examined geographical subdivision of the thiotrophic endosymbionts hosted by Bathymodiolus mussels living along the eastern Pacific hydrothermal vents. High-throughput sequencing data of 16S ribosomal RNA encoding gene and fragments of six protein-coding genes of symbionts were examined in the samples collected from nine vent localities at the East Pacific Rise, Galápagos Rift, and Pacific-Antarctic Ridge.ResultsBoth of the parapatric sister-species, B. thermophilus and B. antarcticus, hosted the same numerically dominant phylotype of thiotrophic Gammaproteobacteria. However, sequences from six protein-coding genes revealed highly divergent symbiont lineages living north and south of the Easter Microplate and hosted by these two Bathymodiolus mussel species. High heterogeneity of symbiont haplotypes among host individuals sampled from the same location suggested that stochasticity associated with initial infections was amplified as symbionts proliferated within the host individuals. The mussel species presently contact one another and hybridize along the Easter Microplate, but the northern and southern symbionts appear to be completely isolated. Vicariance associated with orogeny of the Easter Microplate region, 2.5-5.3 million years ago, may have initiated isolation of the symbiont and host populations. Estimates of synonymous substitution rates for the protein-coding bacterial genes examined in this study were 0.77-1.62%/nucleotide/million years.ConclusionsOur present study reports the most comprehensive population genetic analyses of the chemosynthetic endosymbiotic bacteria based on high-throughput genetic data and extensive geographical sampling to date, and demonstrates the role of the geographical features, the Easter Microplate and geographical distance, in the intraspecific divergence of this bacterial species along the mid-ocean ridge axes in the eastern Pacific. Altogether, our results provide insights into extrinsic and intrinsic factors affecting the dispersal and evolution of chemosynthetic symbiotic partners in the hydrothermal vents along the eastern Pacific Ocean.

Project description:BackgroundExtreme environments prompt the evolution of characteristic adaptations. Yet questions remain about whether radiations in extreme environments originate from a single lineage that masters a key adaptive pathway, or if the same features can arise in parallel through convergence. Species endemic to deep-sea hydrothermal vents must accommodate high temperature and low pH. The most successful vent species share a constrained pathway to successful energy exploitation: hosting symbionts. The vent-endemic gastropod genus Gigantopelta, from the Southern and Indian Oceans, shares unusual features with a co-occurring peltospirid, the 'scaly-foot gastropod' Chrysomallon squamiferum. Both are unusually large for the clade and share other adaptive features such as a prominent enlarged trophosome-like oesophageal gland, not found in any other vent molluscs.ResultsTransmission electron microscopy confirmed endosymbiont bacteria in the oesophageal gland of Gigantopelta, as also seen in Chrysomallon. They are the only known members of their phylum in vent ecosystems hosting internal endosymbionts; other vent molluscs host endosymbionts in or on their gills, or in the mantle cavity. A five-gene phylogenetic reconstruction demonstrated that Gigantopelta and Chrysomallon are not phylogenetically sister-taxa, despite their superficial similarity. Both genera have specialist adaptations to accommodate internalised endosymbionts, but with anatomical differences that indicate separate evolutionary origins. Hosting endosymbionts in an internal organ within the host means that all resources required by the bacteria must be supplied by the animal, rather than directly by the vent fluid. Unlike Chrysomallon, which has an enlarged oesophageal gland throughout post-settlement life, the oesophageal gland in Gigantopelta is proportionally much smaller in juveniles and the animals likely undergo a trophic shift during ontogeny. The circulatory system is hypertrophied in both but the overall size is smaller in Gigantopelta. In contrast with Chrysomallon, Gigantopelta possesses true ganglia and is gonochoristic.ConclusionsKey anatomical differences between Gigantopelta and Chrysomallon demonstrate these two genera acquired a similar way of life through independent and convergent adaptive pathways. What appear to be the holobiont's adaptations to an extreme environment, are driven by optimising bacteria's access to vent nutrients. By comparing Gigantopelta and Chrysomallon, we show that metazoans are capable of rapidly and repeatedly evolving equivalent anatomical adaptations and close-knit relationships with chemoautotrophic bacteria, achieving the same end-product through parallel evolutionary trajectories.

Dataset Information

Classical and computed tomographic anatomical analyses in a not-so-cryptic Alviniconcha species complex from hydrothermal vents in the SW Pacific.

Publications

Classical and computed tomographic anatomical analyses in a not-so-cryptic <i>Alviniconcha</i> species complex from hydrothermal vents in the SW Pacific.

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