Scaling the high latitudes: evolution, diversification, and dispersal of Coryphella nudibranchs across the Northern Hemisphere.

Nudibranch molluscs Coryphella are widely distributed and species-rich gastropod group lacking fossil record and displaying a complex distribution across both Southern and Northern hemispheres. In this paper we provide a detailed review of the morphology, ecology, and distribution of Coryphella, estimation of divergence times between species, an ancestral area reconstruction, and a population analysis of widely distributed trans-Arctic species Coryphella verrucosa to investigate the evolution, phylogeographic patterns and reconstruct possible historical routes of oceanic dispersal. The inclusion of a larger sample size and five molecular markers has revealed a complex evolutionary history of Coryphella, shaped by transgression, vicariance, and dietary shifts, and overall driven by the pervasive effect of glacial cycles. We also revealed the presence of additional cryptic diversity, which suggests that further sampling may produce additional species in this group of nudibranchs. Tree calibration indicates the genus Coryphella originates in the middle Miocene in the Pacific Ocean and the early divergence within this group also occurred in the Pacific, specifically in different regions of the North Pacific. The ancestral area reconstruction inferred five independent instances of transgression from the Pacific Ocean to the Atlantic via different migration routes, including the Panamanian seaway and the Bering Strait. Among them, we identified three cases of successful transition to the Arctic waters from the North Pacific via the Bering Strait, associated with interglacial conditions of middle Pleistocene. Consequently, Pleistocene glacial cycles likely prompted pulses of boreal faunal elements to disperse southwards followed by range disjunction and temporary isolation of distant populations and resulting in allopatric speciation. Evidence from the population structure of contemporary trans-Arctic species suggests an occurrence of independent recolonization pathways of Arctic waters from both southernly and northernly refugia after the Last Glacial Maximum.

Genetic features of bivalve transmissible neoplasia in blue mussels from the Kola Bay (Barents Sea) suggest a recent trans-Arctic migration of the cancer lineages.

Ecology and biogeography of bivalve transmissible neoplasia (BTN) are underexplored due to its recent discovery and a challenging diagnostics. Blue mussels harbour two evolutionary lineages of BTN, MtrBTN1 and MtrBTN2, both derived from Mytilus trossulus. MtrBTN1 has been found only in M. trossulus from North Pacific. MtrBTN2 parasitizes different Mytilus spp. worldwide. BTN in M. trossulus in the Atlantic sector has never been studied. We looked for BTN in mussels from the Barents Sea using flow cytometry of cells, qPCR with primers specific to cancer-associated alleles and sequencing of mtDNA and nuclear loci. Both MtrBTN1 and MtrBTN2 were present in our material, though their prevalence was low (~0.4%). All cancers parasitized M. trossulus except one, MtrBTN1, which was found in a hybrid between M. trossulus and M. edulis. The mtDNA haplotypes found in both lineages were nearly identical to those known from the Northwest Pacific but not from elsewhere. Our results suggest that these two lineages may have arrived in the Barents Sea in recent decades with the maritime transport along the Northern Sea Route. A young evolutionary age of MtrBTN1 seems to indicate that it is an emerging disease in the process of niche expansion. Comparing the new and the published sequence data on tumour suppressor p53, we proved that the prevalence of BTN in mussels can reach epizootic levels. The finding of diverse recombinants between paternally and maternally inherited mtDNAs in somatic tissues of M. trossulus was an unexpected result of our study.

Recalibrating the molecular clock for Arctic marine invertebrates based on DNA barcodes 1.

Divergence times for species assemblages of Arctic marine invertebrates have often been estimated using a standard rate (1.4%/MY) of molecular evolution calibrated using a single sister pair of tropical crustaceans. Because rates of molecular evolution vary among taxa and environments, it is essential to obtain clock calibrations from northern lineages. The recurrent opening and closure of the Bering Strait provide an exceptional opportunity for clock calibration. Here, we apply the iterative calibration approach to investigate patterns of molecular divergence among lineages of northern marine molluscs and arthropods using publicly available sequences of the cytochrome c oxidase subunit I (COI) gene and compare these results with previous estimates of trans-Bering divergences for echinoderms and polychaetes. The wide range of Kimura two-parameter (K2P) divergences among 73 trans-Bering sister pairs (0.12%-16.89%) supports multiple pulses of migration through the Strait. Overall, the results indicate a rate of K2P divergence of 3.2%/MY in molluscs, 5%-5.2%/MY in arthropods, and 3.5%-4.7%/MY in polychaetes. While these rates are considerably higher than the often-adopted 1.4%/MY rate, they are similar to calibrations (3%-5%/MY) in several other studies of marine invertebrates. This upward revision in rates means there is a need both to reevaluate the evolutionary history of marine lineages and to reexamine the impact of prior climatic changes upon the diversification of marine life.

Trans-Arctic vicariance in Strongylocentrotus sea urchins.

The sea urchins Strongylocentotus pallidus and S. droebachiensis first invaded the Atlantic Ocean from the Pacific following the opening of the Bering seaway in the late Miocene. While trans-Arctic dispersal during the Pleistocene is thought to have maintained species' integrity, a recent genomic analysis identified a reproductively isolated cryptic species within S. droebachiensis. Based on previous studies, the distribution of one of these lineages (S. droebachiensis W) includes the shallow water habitats of the northwest Atlantic and Pacific, while the other (S. droebachiensis E) is found throughout the shallow habitat in the northeast but is mostly restricted to deep habitats (>65 m) in the northwest Atlantic. However, since genetic variation within S. droebachiensis has been largely unstudied in the north Pacific and Arctic oceans, the biogeography of the cryptic species is not well known, and it is difficult to identify the mechanisms driving population subdivision and speciation. Here we use population genetic analyses to characterize the distribution of each species, and to test hypotheses about the role of vicariance in the evolution of systematic and genomic divergence within the genus. We collected individuals of all three Strongylocentrotus species (n = 365) from 10 previously unsampled locations in the northeast Pacific and north Atlantic (Labrador Sea and Norway), and generated mtDNA sequence data for a 418 bp fragment of cytochrome c oxidase subunit I (COI). To assess the biogeography of all three species, we combined our alignment with five previously published data sets (total n = 789) and used statistical parsimony and maximum likelihood to identify species and characterize their distribution within and among oceans. Patterns of haplotype sharing, pairwise F ST , and hierarchical analyses of molecular variance (AMOVA) identified trans-Arctic dispersal in S. pallidus and S. droebachiensis W, but other than 5 previously reported singletons we failed to detect additional mtDNA haplotypes of S. droebachiensis E in the north Pacific. Within the Atlantic, patterns of habitat segregation suggests that temperature may play a role in limiting the distribution of S. droebachiensis E, particularly throughout the warmer coastal waters along the coast of Nova Scotia. Our results are consistent with the cycles of trans-Arctic dispersal and vicariance in S. pallidus and S. droebachiensis W, but we suggest that the evolution of Atlantic populations of S. droebachiensis E has been driven by persistent trans-Arctic vicariance that may date to the initial invasion in the late Pliocene.

POPULATION BIOLOGY OF THE TRANS-ARCTIC EXCHANGE: MtDNA SEQUENCE SIMILARITY BETWEEN PACIFIC AND ATLANTIC SEA URCHINS.

MtDNAs from 2 protein coding regions comprising 576 base pairs were sequenced from 17 individual sea urchins of the species Strongylocentrotus pallidus collected from the north Pacific and north Atlantic oceans. Twelve of 17 individual sequences were identical. Two of these were further sequenced in a third, 441 base pair region, and were also found to be identical. We show how to interpret these results using a simplified Markov model of mtDNA evolution at silent sites. The model was calibrated using 3 urchin species with a published fossil record, and shows that identical S. pallidus mtDNAs in different oceans shared a common ancestor at most 90,000-150,000 years ago (95% confidence interval of upper limit of divergence). The Markov model, used to examine patterns of genetic distance within and between species, shows unexpected variation in the rate of base substitution. The rate of change of G's at fourfold sites is nearly 20 times greater than the rate of change of C's. At twofold sites, this range is less extreme, although purines consistently have a higher rate of change than pyrimidines. Striking genetic similarity and recent genetic exchange between oceans for these urchins is in marked contrast to most other trans-Arctic marine populations, which usually show morphological and genetic differentiation at the species or subspecies level. Recent fossil evidence shows that the north Atlantic and northeastern Pacific have been the scene of radical faunal changes during the Pliocene and Pleistocene. The genetic results presented here extend this conclusion to intraspecific patterns of genetic variability, and direct attention to the northwest Pacific where higher productivity and less environmental change may have left a heritage of greater marine genetic diversity.