Population substructure and signals of divergent adaptive selection despite admixture in the sponge Dendrilla antarctica from shallow waters surrounding the Antarctic Peninsula

Abstract

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.

Detecting glacial refugia in the Southern Ocean

“…In Southern Ocean population genetic studies, SNPs have been employed to investigate the population divergence in the sponge Dendrilla antarctica (Leiva et al 2019), the brittle stars Ophionotus victoriae (Galaska et al 2017) and Astrotoma agassizii (Galaska et al 2017), N. australe (Collins et al 2018), and the speciation processes within the P. patagonica species complex (Dömel et al 2019). The use of SNPs could also be useful for investigating past AIS configurations with respect to changes in past patterns of population connectivity and demography (Strugnell et al 2018).…”

The relationship between microbiomes and selective regimes in the sponge genusIrcinia

“…Immune system genes are routinely subjects of balancing selection given the positive effect allelic diversity has in guarding against novel cellular assaults and in detecting a broader suite of foreign epitopes [64], and have been previously detected as being under balancing selection in sponges [65]. In our dataset, we detected multiple outliers under balancing selection involved in immune responses.…”

“…Both balancing and positive selection were detected in viral recombination genes, providing the second account of selection in genes of a viral origin in sponge hosts [65].…”

Microbiomes and host genetics provide evidence for ecological diversification among Caribbean members of the sponge genusIrciniaNardo, 1833

“…After applying population and sample constraints, 266 variant sites (SNPs) remained, each sourced from an independent locus. This volume of SNPs is commensurate with the only other RADseq dataset published to date, whereby 577 SNPs were obtained from 62 individuals of Dendrilla antarctica after filtering out loci that were not present in at least 40% of the individuals(Leiva et al, 2019). The percent of missing data per specimen in our final SNP matrix was 17.3% +/-14.2%.…”