Survival of the fittest: a marine snail toughs it out through a salty time

Dendropoma and its its associated calcareous algae Neogoniolithon brassica-florida. Photo from the Mediterranean Sea climate and environmental change blog

The vermetid gastropod Dendropoma and its its associated calcareous algae Neogoniolithon brassica-florida. Photo from the Mediterranean Sea climate and environmental change blog.

For marine organisms, salinity plays an important role in determining how populations and species are distributed across time and space, particularly in the Mediterranean Sea. During the Mesozoic, about 252 to 66 million years ago, the Tethys Ocean, a body of water that would become the Mediterranean Sea, connected the Atlantic and Pacific oceans. According to Lejeusne et al., “the Mediterranean is a peculiar sea, a product of a tormented geological history, where continents collide and water masses come and go, a crossroads of biogeographical influences between cold temperate biota and subtropical species.”

In the Miocene, about 5.96 to 5.33 million years ago, the Mediterranean went through a cyclical desiccation event called the Messinian Salinity Crisis (MSC) during which the Straits of Gibraltar closed and the sea was reduced to a series of hyper-saline and brackish water lakes. The crisis ended when wetter conditions allowed for more freshwater flow from rivers into the basin and the Straits of Gibraltar reopened, flooding the region with water from the eastern Atlantic. The MSC caused mass extinctions in Mediterranean and there is little evidence that any fully marine species survived through the MSC in this region. For a great set of blog posts on the MSC (with cool images and figures), click here.

In their recent Molecular Phylogenetics and Evolution paper, Calvo and Alda et al. (2015) infer phylogenetic relationships and date lineage divergences in a vermetid gastropod, Dendropoma petraeum, endemic to the Mediterranean Sea. Using mitochondrial and nuclear loci the authors uncovered four morphologically cryptic lineages distributed geographically and phylogenetically west to east across the Mediterranean (each lineage is represented by a different color in the figure below).

Fig. 1. Sampling localities and distribution of the main lineages identified in Dendropoma petraeum. Locality codes as indicated in Table 1. Colors represent lineages: Western (orange), Tyrrhenian (green), Ionian-Aegean (blue), Levantine (pink).

Fig. 1. Sampling localities and distribution of the main lineages identified in Dendropoma petraeum. Locality codes as indicated in Table 1. Colors represent lineages: Western (orange), Tyrrhenian (green), Ionian-Aegean (blue), Levantine (pink). Figure and caption from Calvo and Alda et al.

Calvo and Alda et al. calibrated a molecular clock under two alternative biogeographical scenarios and estimated substitution rates under each hypothesis: (1) D. petraeum survived the MSC and its major lineages diverged during this period versus (2) D. petraeum did NOT survive the MSC and recolonized the Mediterranean after that period. The authors tested which hypothesis best fit their data using Bayes factors.

Divergence dating placed the first split (mean values) at 10.09 million years ago and two subsequent splits that yielded the 4 lineages observed today at 8.14 (blue and pink lineages split) and 7.86 million years ago (orange and green split), although the highest posterior density ranges for the divergences overlapped. Within lineage diversification events in all four lineages occurred more recently between 3.57 and 0.52 million years ago.

Fig. 3. Species tree based on the multispecies coalescent implemented in ⁄BEAST and obtained for the complete data set of mitochondrial and nuclear data. Node bars represent 95% highest posterior densities (HPD) of the estimated divergence time between lineages, and bars on branches represent 95% HPD of time estimated tMRCA within lineages. Dashed-lined squares represent the two main periods of diversification discussed in text. The gray square indicates the Messinian Salinity Crisis (MSC). Figure and caption from Calvo and Alda et al.

Fig. 3. Species tree based on the multispecies coalescent implemented in ⁄BEAST and obtained for the complete data set of mitochondrial and nuclear data. Node bars represent 95% highest posterior densities (HPD) of the estimated divergence time between lineages, and bars on branches represent 95% HPD of time estimated tMRCA within lineages. Dashed-lined squares represent the two main periods of diversification discussed in text. The gray square indicates the Messinian Salinity Crisis (MSC). Figure and caption from Calvo and Alda et al.

In contrast to the similarities in lineage diversification, patterns demographic change and spatial genetic structure varied across lineages. Extended Bayesian skyline plots showed the westernmost lineages were characterized by historical increases in population size while size remained constant in the eastern lineages. Genetic distance generally increased with geographic distance in the orange and blue lineages, but not in the green or purples ones.

Bayes factors and divergence dating by Calvo and Alda et al. suggest D. petraeum made it through the MSC.

…Our estimates indicate that the divergence time between the different species of Dendropoma in the Mediterranean predates or coincides with the MSC suggesting that they would have survived this dramatic period within this sea in isolated refugia, at least the Tyrrhenian–Sicilian [green], Ionian–Aegean [blue] and Levantine [pink] species.

Dendropoma could have survived in refugia in the westernmost Mediterranean close to the Atlantic and/or in the eastern end of the basin where more hospitable conditions existed. These refugia would have likely facilitated divergence among lineages.

Isolation of the eastern Mediterranean refugia may have been accompanied by reduction of their population sizes, enhancing divergence in allopatry of the isolated populations, and in turn resulting in incipient speciation.

Given their “mid-Messinian” divergences, the cryptic Dendropoma species could be considered paleo-endemisms, likely of Tethyan origin, in contrast to the neo-endemisms of Pliocene origin, which constitute most of present-day endemic species in the Mediterranean.

References

Calvo, Marta, Fernando Alda, Marco Oliverio, José Templado, and Annie Machordom (2015) Surviving the Messinian Salinity Crisis? Divergence patterns in the genus Dendropoma (Gastropoda: Vermetidae) in the Mediterranean Sea. Molecular Phylogenetics and Evolution91, 17-26. DOI: 10.1016/j.ympev.2015.05.004

Lejeusne, Christophe, Pierre Chevaldonné, Christine Pergent-Martini, Charles F. Boudouresque, and Thierry Perez (2010) Climate change effects on a miniature ocean: the highly diverse, highly impacted Mediterranean Sea. Trends in Ecology & Evolution25, 250-260. DOI: 10.1016/j.tree.2009.10.009

Hsü, K. J., W. B. F. Ryan, and M. B. Cita (1973) Late Miocene desiccation of the Mediterranean. Nature 24, 2240-244. DOI: 10.1038/242240a0

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About Melissa DeBiasse

I am a postdoctoral researcher at the University of Florida Whitney Laboratory for Marine Bioscience. As an evolutionary ecologist I am interested in the processes that generate biodiversity in marine ecosystems. My research uses experimental methods and genomic and phenotypic data to test how marine invertebrate species respond to biotic and abiotic stressors over ecological and evolutionary timescales.
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