Description: Highlights: • Fan-shaped sponges display panmixia at three locations in the Cantabrian Sea. • Subtle sponge population genetic and pronounced microbial differences were observed between a canyon and bank (〈100km apart). • Lagrangian modelling reveals variable inter-annual connectivity via ocean currents between the sampling regions. • Interdisciplinary approaches can help to improve understanding about connectivity in the deep-sea. Abstract: Connectivity is a fundamental process driving the persistence of marine populations and their adaptation potential in response to environmental change. In this study, we analysed the population genetics of two morphologically highly similar deep-sea sponge clades (Phakellia hirondellei and the ‘Topsentia-and-Petromica’ clade, (hereafter referred to as ‘TaP clade’)) at three locations in the Cantabrian Sea and simultaneously assessed the corresponding host microbiome by 16S rRNA gene sequencing. A virtual particle tracking approach (Lagrangian modelling) was applied to assess oceanographic connectivity in the study area. We observed overall genetic uniformity for both sponge clades. Notably, subtle genetic differences were observed for sponges of the TaP clade and also their microbiomes between a canyon and bank location, 〈 100 km apart and with the same depth range. The Lagrangian model output suggests a strong retention of larvae in the study area with variable inter-annual connectivity via currents between the three sampling regions. We conclude that geologic features (canyons) and the prevailing ocean currents may dictate sponge holobiont connectivity and that differentiation can emerge even on small spatial scales.

Description: Highlights: • First time hybridization is detected in deep-water sponges (Phakellia) using SNPs. • Hybridization corroborated by morphological and microbial analyses. • Connectivity between shallow populations of Phakellia robusta spanning ca. 2,000 km. • Molecular connectivity explained by prevalent oceanographic currents. Abstract: Deep-sea North Atlantic sponge grounds are crucial components of the marine fauna providing a key role in ecosystem functioning. To properly develop effective conservation and management plans, it is crucial to understand the genetic diversity, molecular connectivity patterns and turnover at the population level of the species involved. Here we present the study of two congeneric sponges, Phakellia robusta and Phakellia hirondellei, using multiple sources of evidence. Our phylogenetic study using a fragment of COI placed these two species as sister. Haplotype network analysis using COI revealed no genetic structure for P. hirondellei in samples from the Cantabrian Sea (〈100 km). Contrastingly, P. robusta showed a clear genetic structure separating deep-water samples from the Cantabrian Sea and the Hatton-Rockall Basin, from samples from shallower waters from Kerry Head Reefs, NW of Orkney, and Norway. ddRADSeq-derived SNPs for P. robusta also segregated samples by bathymetry rather than by geographical distances, and detected a predominant northwards migration for shallow-water specimens connecting sites separated ca. 2,000 km, probably thanks to prevalent oceanographic currents. Importantly, our analysis using SNPs combining the datasets of the two species revealed the presence of potential hybrids, which was corroborated by morphological (spicule) and microbial (16S amplicon sequencing) analyses. Our data suggest that hybridization between these two species occurred at least two times in the past. We discuss the importance of using next-generation techniques to unveil hybridization and the implications of our results for conservation.