Genome-wide phylogeography reveals cryptic speciation in the circumglobal planktonic calcifier Limacina bulimoides.

Little is known about when and how planktonic species arise and persist in the open ocean without apparent dispersal barriers. Pteropods are planktonic snails with thin shells susceptible to dissolution that are used as bio-indicators of ocean acidification. However, distinct evolutionary units respond to acidification differently, and defining species boundaries is therefore crucial for predicting the impact of changing ocean conditions. In this global population genomic study of the shelled pteropod Limacina bulimoides, we combined genetic (759,000 single nucleotide polymorphisms) and morphometric data from 161 individuals, revealing three major genetic lineages (FST = 0.29-0.41): an "Atlantic lineage" sampled across the Atlantic, an "Indo-Pacific lineage" sampled in the North Pacific and Indian Ocean, and a "Pacific lineage" sampled in the North and South Pacific. A time-calibrated phylogeny suggests that the lineages diverged about 1 million years ago, with estimated effective population size remaining high (~10 million) throughout Pleistocene glacial cycles. We do not observe any signatures of recent hybridization, even in areas of sympatry in the North Pacific. While the lineages are reproductively isolated, they are morphologically cryptic, with overlapping shell shape and shell colour distributions. Despite showing that the circumglobal L. bulimoides consists of multiple species with smaller ranges than initially thought, we found that these pteropods still possess high levels of genetic variability. Our study adds to the growing evidence that speciation is often overlooked in the open ocean, and suggests the presence of distinct biological species within many other currently defined circumglobal planktonic species.

Pteropods are excellent recorders of surface temperature and carbonate ion concentration.

Pteropods are among the first responders to ocean acidification and warming, but have not yet been widely explored as carriers of marine paleoenvironmental signals. In order to characterize the stable isotopic composition of aragonitic pteropod shells and their variation in response to climate change parameters, such as seawater temperature, pteropod shells (Heliconoides inflatus) were collected along a latitudinal transect in the Atlantic Ocean (31° N to 38° S). Comparison of shell oxygen isotopic composition to depth changes in the calculated aragonite equilibrium oxygen isotope values implies shallow calcification depths for H. inflatus (75 m). This species is therefore a good potential proxy carrier for past variations in surface ocean properties. Furthermore, we identified pteropod shells to be excellent recorders of climate change, as carbonate ion concentration and temperature in the upper water column have dominant influences on pteropod shell carbon and oxygen isotopic composition. These results, in combination with a broad distribution and high abundance, make the pteropod species studied here, H. inflatus, a promising new proxy carrier in paleoceanography.

Genetic architecture in a marine hybrid zone: comparing outlier detection and genomic clines analysis in the bivalve Macoma balthica.

The role of natural selection in speciation has received increasing attention and support in recent years. Different types of approaches have been developed that can detect genomic regions influenced by selection. Here, we address the question whether two highly different methods--F(ST) outlier analysis and admixture analysis--detect largely the same set of non-neutral genomic elements or, instead, complementary sets. We study genetic architecture in a natural secondary contact zone where extensive admixture occurs. The marine bivalves Macoma balthica rubra and M. b. balthica descend from two independent trans-Arctic invasions of the north Atlantic and hybridize extensively where they meet, for example in the Kattegat-Danish Straits-Baltic Sea region. The Kattegat-Danish Straits region forms a steep salinity cline and is the only entrance to the recently (ca. 8000 years ago) established brackish water basin the Baltic Sea. Salinity along the contact zone drops from 30‰ (Skagerrak, M.b.rubra) to 3‰ (Baltic, M.b.balthica). Both outlier analysis and genomic clines analysis suggest that large parts of the genome are influenced by non-neutral effects. Contrasting samples from well outside the hybrid zone, outlier analysis detects 16 of 84 amplified fragment length polymorphism markers as significant F(ST) outliers. Genomic clines analysis detects 31 of 84 markers as non-neutral inside the hybrid zone. Remarkably, only three markers are detected by both methods. We conclude that the two methods together identify a suite of markers that are under the influence of non-neutral effects.

Spatial and temporal genetic structure of the planktonic Sagitta setosa (Chaetognatha) in European seas as revealed by mitochondrial and nuclear DNA markers.

Little is known about the spatial and temporal scales at which planktonic organisms are genetically structured. A previous study of mitochondrial DNA (mtDNA) in the holoplanktonic chaetognath Sagitta setosa revealed strong phylogeographic structuring suggesting that Northeast (NE) Atlantic, Mediterranean and Black Sea populations are genetically disjunct. The present study used a higher sampling intensity and a combination of mitochondrial and four microsatellite markers to reveal population structuring between and within basins. Between basins, both marker sets indicated significant differentiation confirming earlier results that gene flow is probably absent between the respective S. setosa populations. At the within-basin scale, we found no evidence of spatial or temporal structuring within the NE Atlantic. In the Mediterranean basin, both marker sets indicated significant structuring, but only the mtDNA data indicated a sharp genetic division between Adriatic and all other Mediterranean populations. Data were inconclusive about population structuring in the Black Sea. The levels of differentiation indicated by the two marker sets differed substantially, with far less pronounced structure detected by microsatellite than mtDNA data. This study also uncovered the presence of highly divergent mitochondrial lineages that were discordant with morphology, geography and nuclear DNA. We thus propose the hypothesis that highly divergent mitochondrial lineages may be present within interbreeding S. setosa populations.