Sponge diversification in marine lakes: Implications for phylogeography and population genomic studies on sponges

Abstract

The relative influence of geography, currents, and environment on gene flow within sessile marine species remains an open question. Detecting subtle genetic differentiation at small scales is challenging in benthic populations due to large effective population sizes, general lack of resolution in genetic markers, and because barriers to dispersal often remain elusive. Marine lakes can circumvent confounding factors by providing discrete and replicated ecosystems. Using high-resolution double digest restriction-site-associated DNA sequencing (4826 Single Nucleotide Polymorphisms, SNPs), we genotyped populations of the sponge Suberites diversicolor (n = 125) to test the relative importance of spatial scales (1-1400 km), local environmental conditions, and permeability of seascape barriers in shaping population genomic structure. With the SNP dataset, we show strong intralineage population structure, even at scales <10 km (average F _ST = 0.63), which was not detected previously using single markers. Most variation was explained by differentiation between populations (AMOVA: 48.8%) with signatures of population size declines and bottlenecks per lake. Although the populations were strongly structured, we did not detect significant effects of geographic distance, local environments, or degree of connection to the sea on population structure, suggesting mechanisms such as founder events with subsequent priority effects may be at play. We show that the inclusion of morphologically cryptic lineages that can be detected with the COI marker can reduce the obtained SNP set by around 90%. Future work on sponge genomics should confirm that only one lineage is included. Our results call for a reassessment of poorly dispersing benthic organisms that were previously assumed to be highly connected based on low-resolution markers.

Keywords: Porifera; RADseq; Suberites diversicolor; genetic resolution; marine biodiversity; seascape genomics.

FIGURE 1

Sampling sites of Suberites diversicolor from nine marine lakes and two lagoon locations and associated relative migration networks. (a) Overview of Indonesia including two geographic regions sampled: Berau, East‐Kalimantan and Raja Ampat, West‐Papua. It also shows the location of the Australian lagoon sampled (Sea Australia). (b) Zoom of Berau, with locations of three marine lakes (Kalimantan1, Kalimantan2, and Kalimantan3) and one lagoon (Sea Indonesia). (c) Zoom of Raja Ampat, with locations of six marine lakes (Papua27, Papua30, Papua32, Papua1, Papua4, and Papua5). (d) Relative migration network including only samples from Lineage B based on 4826 SNPs and run with 1000 bootstraps. Fractions of relative migration are displayed and categories of level of connection to the surrounding sea are indicated. (e) Specimen of S. diversicolor, photograph by L.E. Becking.

FIGURE 2

Distinction of major genetic lineages A and B of sponge populations. (a) Maximum Likelihood IQTree using consensus sequences of 125 individuals based on 541 SNPs. Bootstrap values for major branches are displayed. (b) Bayesian admixture analysis for putative ancestral populations (K 7–11) based on genotype likelihoods via ngsAdmix. Each bar represents one individual. K = 9 was indicated as the most likely ancestral populations. (c) Analysis of Molecular Variance (AMOVA) for Lineage A and B (top), and only Lineage B (bottom). Amount of variance explained in percentage, F‐values and significance values are displayed. Colors and codes correspond to Figure 1 and Table 1.

FIGURE 3

Population genomic structure analyses for Lineage B from sponge populations. (a) Principal Component Analysis (PCA) based on pairwise covariance. Each dot represents one individual. (b) Neighbor‐Joining Network with equal angles computed in Splitstree based on pairwise genomic distances. (c) Heatmap of normalized F'_ST (values in Table S5). Colors and codes correspond to Figure 1 and Table 1.

FIGURE 4

Demographic history inferences on sponge populations within Lineage B. Demographic histories of six locations are displayed: lagoon populations Sea Indonesia and Sea Australia (top), highly connected marine lakes Papua 4 and Papua30 (middle), and isolated lakes Papua1 and Papua5 (bottom). Mean (dark) and 12.5/87.5% confidence intervals are displayed. The gray box indicates putative filling of marine lakes after the Last Glacial Maximum (8000–10,000 years ago).