Striking genetic structure among marine populations at small spatial scales is becoming evident with extensive molecular studies. Such observations suggest isolation at small scales may play an important role in forming patterns of genetic diversity within species. Isolation-by-distance, isolation-by-environment and historical priority effects are umbrella terms for a suite of processes that underlie genetic structure, but their relative importance at different spatial and temporal scales remains elusive. Here, we use marine lakes in Indonesia to assess genetic structure and assess the relative roles of the processes in shaping genetic differentiation in populations of a bivalve mussel (Brachidontes sp.). Marine lakes are landlocked waterbodies of similar age (6,000-10,000 years), but with heterogeneous environments and varying degrees of connection to the sea. Using a population genomic approach (double-digest restriction-site-associated DNA sequencing), we show strong genetic structuring across populations (range F : 0.07-0.24) and find limited gene flow through admixture plots. At large spatial scales (>1,400 km), a clear isolation-by-distance pattern was detected. At smaller spatial scales (<200 km), this pattern is maintained, but accompanied by an association of genetic divergence with degree of connection. We hypothesize that (incomplete) dispersal barriers can cause initial isolation, allowing priority effects to give the numerical advantage necessary to initiate strong genetic structure. Priority effects may be strengthened by local adaptation, which the data may corroborate by showing a high correlation between mussel genotypes and temperature. Our study indicates an often-neglected role of (evolution-mediated) priority effects in shaping population divergence.

Marine lakes, with populations in landlocked seawater and clearly delineated contours, have the potential to provide a unique model to study early stages of evolution in coastal marine taxa. Here we ask whether populations of the mussel Brachidontes from marine lakes in Berau, East Kalimantan (Indonesia) are isolated from each other and from the coastal mangrove systems. We analyzed sequence data of one mitochondrial marker (Cytochrome Oxidase I (COI)), and two nuclear markers (18S and 28S). In addition, we examined shell shape using a geometric morphometric approach. The Indonesian populations of Brachidontes spp. harbored four deeply diverged lineages (14–75% COI corrected net sequence divergence), two of which correspond to previously recorded lineages from marine lakes in Palau, 1,900 km away. These four lineages also showed significant differences in shell shape and constitute a species complex of at least four undescribed species. Each lake harbored a different lineage despite the fact that the lakes are separated from each other by only 2–6 km, while the two mangrove populations, at 20 km distance from each other, harbored the same lineage and shared haplotypes. Marine lakes thus represent isolated habitats. As each lake contained unique within lineage diversity (0.1–0.2%), we suggest that this may have resulted from in situdivergence due to isolation of founder populations after the formation of the lakes (6,000–12,000 years before present). Combined effects of stochastic processes, local adaptation and increased evolutionary rates could produce high levels of differentiation in small populations such as in marine lake environments. Such short-term isolation at small spatial scales may be an important contributing factor to the high marine biodiversity that is found in the Indo-Australian Archipelago.

AimStudying clearly delineated populations in marine lakes, islands of sea, we investigated the interplay of habitat size, dispersal potential, and priority effects in shaping marine population genetic structure.LocationMarine lakes and coastal locations in Indonesia, Palau, Papua New Guinea and Australia.TaxonMussels (Mytilidae, Brachidontes spp.)MethodsPopulations were sampled from four coastal locations and 22 marine lakes of similar age (~8,000 years), yet differing in size (0.04–4.7 km2) and degree of connection to the adjacent sea. While some lakes are highly connected, allowing potential influx of larvae from the sea, others have very limited water exchange. We assessed the phylogeographical structure and demographic history using mitochondrial and nuclear DNA sequence data, and combined this with geometric morphometrics. The effects of lake characteristics on population genetic diversity and structure were tested using linear regression and Mantel tests.ResultsEach lake contained one of six distinct genetic lineages, which were characterized by deep phylogenetic splits and significant morphometric differences. These lineages likely represent separate species. The lineages showed similar demographic patterns, with lakes containing founder populations that rapidly expanded and diverged. Genetic diversity within lake populations was significantly correlated with lake area, but not with physical connection to the adjacent sea. Within lineages that occurred in multiple lakes there was strong population structure (average ΦST 0.65), which did not conform to an isolation‐by‐distance pattern or to the degree of dispersal potential.Main ConclusionsMarine lakes across a gradient of physical isolation show strong population structure and evidence for in situ divergence. We hypothesize that the observed genetic structure is the result of priority effects. In addition, reduction of habitat size appears to reduce genetic diversity, even at very small spatial scales. Our findings are relevant in the context of ongoing alterations to coastal hydrodynamics, which lead to habitat reduction and influence migration among populations at fine spatial scales.

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The relative influence of geography, oceanography and environment on gene flow within sessile marine species remains an open question. Detecting subtle genetic differentiation at small scales relevant to marine protected areas is challenging in benthic populations due to large effective population sizes, general lack of resolution in genetic markers, potential microbial associations, and because barriers to dispersal often remain elusive. We genotyped the sponge species Suberites diversicolor using double digest restriction-site associated DNA sequencing (4,826 Single Nucleotide Polymorphisms, SNPs), compared it to same individuals using single markers (COI and ITS), and used previously published data on the associated microbial communities from a subset of the same locations. Studying S. diversicolor from marine lakes at different spatial scales (1-1,400 km), along a gradient of connection to the surrounding sea, and with different environmental regimes, we did not detect strong effects of geographic distance, permeability of seascape barriers or local environments in shaping population genetic structure. All markers detected two major lineages and geographic clustering over a large spatial scale. However, with the SNP dataset we provide new evidence of strong population structure even at scales <10km (average FST = 0.56), where previously none was detected. A lack of congruence between host population structure and microbial community patterns of S. diversicolor from the same locations was observed, suggesting they are on different eco-evolutionary tracks. Our results call for a reassessment of poorly dispersing benthic organisms that were previously assumed to be highly connected based on low resolution markers.

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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.