Antarctic shallow‐water invertebrates are exceptional candidates to study population genetics and evolution, because of their peculiar evolutionary history and adaptation to extreme habitats that expand and retreat with the ice sheets. Among them, sponges are one of the major components, yet population connectivity of none of their many Antarctic species has been studied. To investigate gene flow, local adaptation and resilience to near‐future changes caused by global warming, we sequenced 62 individuals of the sponge Dendrilla antarctica along the Western Antarctic Peninsula (WAP) and the South Shetlands (spanning ~900 km). We obtained information from 577 double digest restriction site‐associated DNA sequencing (ddRADseq)‐derived single nucleotide polymorphism (SNP), using RADseq techniques for the first time with shallow‐water sponges. In contrast to other studies in sponges, our 389 neutral SNPs data set showed high levels of gene flow, with a subtle substructure driven by the circulation system of the studied area. However, the 140 outlier SNPs under positive selection showed signals of population differentiation, separating the central–southern WAP from the Bransfield Strait area, indicating a divergent selection process in the study area despite panmixia. Fourteen of these outliers were annotated, being mostly involved in immune and stress responses. We suggest that the main selective pressure on D. antarctica might be the difference in the planktonic communities present in the central–southern WAP compared to the Bransfield Strait area, ultimately depending on sea‐ice control of phytoplankton blooms. Our study unveils an unexpectedly long‐distance larval dispersal exceptional in Porifera, broadening the use of genome‐wide markers within nonmodel Antarctic organisms.
Most animals, including sponges (Porifera), have species‐specific microbiomes. Which genetic or environmental factors play major roles structuring the microbial community at the intraspecific level in sponges is, however, largely unknown. In this study, we tested whether geographic location or genetic structure of conspecific sponges influences their microbial assembly. For that, we used three sponge species with different rates of gene flow, and collected samples along their entire distribution range (two from the Mediterranean and one from the Southern Ocean) yielding a total of 393 samples. These three sponge species have been previously analysed by microsatellites or single nucleotide polymorphisms, and here we investigate their microbiomes by amplicon sequencing of the microbial 16S rRNA gene. The sponge Petrosia ficiformis, with highly isolated populations (low gene flow), showed a stronger influence of the host genetic distance on the microbial composition than the spatial distance. Host‐specificity was therefore detected at the genotypic level, with individuals belonging to the same host genetic cluster harbouring more similar microbiomes than distant ones. On the contrary, the microbiome of Ircinia fasciculata and Dendrilla antarctica ‐ both with weak population structure (high gene flow) ‐ seemed influenced by location rather than by host genetic distance. Our results suggest that in sponge species with high population structure, the host genetic cluster influence the microbial community more than the geographic location.
Invertebrate and microbial marine communities associated with mammal bones are interesting and poorly understood habitats, mainly known from studies on deep-water whale remains. In order to characterize these communities in the shallow-water Mediterranean, we present here the results of a pioneering experiment using mammal bones. Minke whale, pig and cow bones were experimentally deployed on three different background communities: rocky substrate, soft-bottom and a Posidonia oceanica meadow. Bones were deployed for a year at about 20 m depth and collected every 3 months, and the invertebrate fauna colonizing the bones was identified to the lowest possible taxonomic level. As expected, mammal bones showed remarkable differences when compared with background communities. Within bones, four different clusters could be identified, primarily on the basis of the polychaete fauna, the most abundant and diverse group in the survey. Clusters A1-A3 corresponded to high to moderately altered successional stages composed by a fauna closer to that of anthropogenically enriched shallow-water environments. These clusters were characterized by the occurrence of the opportunist polychaetes Ophryotrocha puerilis, Neanthes caudata (Cluster A1), Protodorvillea kefersteini (Cluster A2) and Ophryotrocha alborana (Cluster A3). Cluster B was characterized by the presence of the polychaete Oxydromus pallidus together with typical invertebrate background fauna, which suggests that this community, after a year of deployment, was closer to that found in natural conditions. As opposed to similar shallow-water studies in other geographic areas, no occurrence of the polychaete Osedax (commonly known as bone-eating worms) was reported from our experiments. Apart from the study on the invertebrate communities, insights about the population dynamics of three of the most abundant species (O. puerilis, O. alborana, N. caudata) are given as well as remarks on a hypothetical trophic network based on fecal pellet analysis.
Shallow‐water polychaetes are abundant and diverse components of the Southern Ocean benthic communities, and although they have been widely studied, new species that are relatively common are still discovered. Here, we report the discovery of Pterocirrus giribeti sp. n., a new and abundant intertidal and upper‐subtidal Antarctic phyllodocid. To establish the phylogenetic relationships of the new species, we sequenced two nuclear (18S and 28S) and two mitochondrial (COI and 16S) markers. Although the phylogenetic relationships obtained for the family Phyllodocidae were not fully resolved, we assigned our new phyllodocid to the genus Pterocirrus based on both its phylogenetic position and its morphological characters. Using COI and 16S sequences of 126 and 118 individuals, respectively, from eight populations across the South Shetland Islands and the Antarctic Peninsula, we also investigated the genetic diversity and gene flow patterns of this new species. Our results suggested that all populations were panmictic, likely due to the presence of planktotrophic larvae allowing long‐distance dispersal. Interestingly, some genetic substructure was detected despite panmixis, and we identified a semipermeable barrier coinciding with an oceanic front produced by the intrusion into the Bransfield Strait of a tongue of water from the Weddell Sea. This front produced signatures of differentiation on populations at the tip of the West Antarctic Peninsula. Moreover, our results indicated a recent demographic expansion throughout the sampled area, in agreement with the “glacial refugium” hypothesis stated for other Antarctic shallow‐water invertebrates.
Syllid annelids from the so-called ‘ribbon clade’ are flattened, ribbon-shaped worms of the genera Parahaplosyllis Hartmann-Schröder, 1990, Eurysyllis Ehlers, 1864, Xenosyllis Marion & Bobretzky, 1875, Trypanosyllis Claparède, 1864, Ramisyllis Glasby, Schroeder & Aguado, 2012, Trypanobia Imajima & Hartman, 1964, Plakosyllis Hartmann-Schröder, 1956, Pseudosyllis Grube, 1863 and Trypanedenta Imajima & Hartman, 1964. Some species possess a remarkable reproductive strategy using multiple stolons that has been recently suggested to be ancestral to the group. Here, to evaluate the evolution of reproductive modes in the group, we assess, for the first time, the phylogenetic relationships within the ribbon clade and related genera. We collected new material of Trypanobia and Trypanosyllis from Japan, Spain, Philippines and Indonesia and sequenced it for the nuclear markers 18S rRNA and the mitochondrial markers 16S rRNA and cytochrome c oxidase I for phylogenetic inference and also performed ancestral character reconstruction for the reproductive strategy in the entire group. Formal taxonomic descriptions of a new genus and six new species are provided. The new genus, Trypanospina, gen. nov., is characterised by the spines that cover its surface. Most genera within the ‘ribbon clade’ are monophyletic and the relationships appeared well supported in most cases. However, our phylogenetic hypotheses are not conclusive in regard to the relationships of the genera Trypanedenta and Trypanobia, nor to the status of those to genera as distinctive, since they seem to be paraphyletic and they appear in low-supported clades. In contrast, our results shed light on the evolution of the reproductive modes within the group, showing that scissiparity (development of a single stolon each time) is the ancestral character for the entire group and gemmiparity (development of more than one stolon at the same time) then appeared twice in two independent clades.
Over the past several years, there has been growing interest in how bones of decaying mammals are colonized in the marine seabed. One of the most common opportunistic taxa occurring worldwide on bones is dorvilleid polychaetes of the genus Ophryotrocha. In a recent study in the Mediterranean, Ophryotrocha puerilis and Ophryotrocha alborana were two of the most abundant species occurring in experimentally deployed bones. These species have direct development and this makes them a suitable model to study the mechanisms and processes allowing organisms lacking a dispersive larval phase to colonize new substrates. Here, we address the colonization processes at the molecular level for populations of O. puerilis and O. alborana on experimentally deployed mammal bones in the shallow‐water Mediterranean collected over a year at 3‐month intervals. High genetic distances between some of the O. puerilis organisms collected indicated the occurrence of at least two cryptic sibling species (O. puerilis ‘Shallow’ and O. puerilis ‘Deep’) apart from O. puerilis sensu stricto. This was corroborated with phylogenetic analyses using an alignment of three concatenated genes (COI, 16S, H3) and with species delimitation analyses using COI. The haplotype network inferred from COI sequences for O. puerilis ‘Shallow’ showed a few common haplotypes shared between the two trimesters analysed and several other less represented haplotypes only present in one trimester. Thus, colonization of these experimental bones may have been achieved by a few organisms that arrived to the bones and were able to reseed, and by several individuals arriving to the experimental bones and not persisting across time. In contrast, the haplotype network for O. alborana revealed that none of the haplotypes present in three different trimesters were shared, suggesting that the populations arriving at the bones during each trimester were totally replaced by new individuals during the subsequent trimesters. Our study suggests that different species of shallow‐water Ophryotrocha occurring in the Mediterranean may have different patterns of substrate colonization despite sharing similar life histories.
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