The boreal faunas of the North Atlantic and North Pacific oceans comprise many instances of closely related, vicariously distributed species pairs, reflecting a history of shared ancestry followed by inter-oceanic isolation through the Pleistocene and Holocene epochs. In most cases, this vicariance is thought to trace back to the Great Trans-Arctic Interchange approximately 3.5 Mya that followed the Pliocene opening of the Bering Strait, until which most of the lineages were restricted to a single ocean basin, and after which the Pleistocene conditions again restricted the dispersal (e.g. [1, 2]). Yet even since that time species could in principle have had several opportunities to disperse through the Arctic. The patterns of biotic exchange have been controlled by the history of climatic and hydrographical circumstances, but also by the thermal tolerance and dispersal characteristics of the taxa. Indeed, phylogeographical studies of amphi-boreal taxa have so far demonstrated a variety of inter-oceanic systematic affinities and more complex isolation/dispersal histories such as repeated trans-Arctic invasions, both in fishes (e.g. [3, 4]) and invertebrates [5, 6].
Among the most prominent pairs of amphi-boreal vicariant taxa are the Pacific and Atlantic herrings, Clupea pallasii Valenciennes, 1847 and Clupea harengus Linnaeus, 1758. They are pelagic planktivores occurring in massive schools and occupying both coasts of their respective oceans, from the temperate up to the subarctic zone. The inter-oceanic vicariance caused by the Arctic dispersal barrier is however not complete, but is broken by the presence of remote populations of C. pallasii in border waters of the NE Atlantic in Europe, particularly in the White and the south-eastern Barents seas. Also the Atlantic C. harengus penetrates these seas from the west, although does not spawn there [7, 8]. Moreover, isolated occurrences of C. pallasii even further west in some Norwegian Sea fjords are known .
The European populations of C. pallasii demonstrate remarkable heterogeneity of their life histories (e.g. ). In the White Sea Gulf of Kandalaksha, a fast-growing summer-spawning form similar to typical Pacific herring is distinguished from a more abundant slow-growing form, which uniquely breeds under the ice in the spring. There are also a number of other herring stocks in other parts of the White Sea and in the south-eastern Barents Sea, which differ in their growth rates and spawning seasons. The origins and status of the seasonal vs. geographical breeding stocks have been debated for decades, but genetic data so far have yielded contradicting results on these issues [11, 12]. At a broader regional scale in NE Europe, a subspecies-level division has generally been recognized, into the White Sea herring C. pallasii marisalbi Berg, 1923, and the Chesha–Pechora herring C. pallasii suworowi Rabinerson, 1927 in the south-eastern Barents Sea .
The timing and the geography of the origin of the European populations remain unexplored in phylogeographic terms, whereas allozyme and initial mitochondrial data have confirmed their Pacific species identity [8, 12, 13]. Based on paleogeographical facts, they have been thought to represent relict populations of a wider geographic distribution that existed along the Eurasian Arctic coast during warmer post-glacial times < 10 ky ago (e.g. ). The European outposts of a Pacific boreal taxon provide a platform to consider the dynamics of trans-Arctic connections in the context of climatic history, and should help to understand the biological consequences of the current climatic warming for integrity of biological diversity in the boreal and arctic seas (cf. [15, 16]).
Here we use the genealogical information in mitochondrial DNA sequence variation to assess the demographic histories and sub-structuring of the amphi-boreal species of herrings at various temporal and geographical scales, and particularly to trace the history and status of the NE European outpost populations of C. pallasii. Recent studies of C. pallasii within the Pacific have corroborated a pronounced intra-basin east–west subdivision, but raised discussion of interpreting the demography from mitochondrial control region data [17, 18]. No comparable broad-scale sequence data exist for the North Atlantic C. harengus, whereas it has appeared genetically relatively homogeneous on oceanic and regional scales in other genetic markers (e.g. [19–21], but see ). As a background, we first assess the mtDNA diversity of the two species in their native basins from comparable datasets. Then focusing on the inter-oceanic dispersal that should account for the presence of C. pallasii in Europe, three main hypotheses of invasion times are considered, i.e. pre-glacial (e.g. during Eemian interglacial period) approximately 120 kya, early post-glacial from the opening of the Bering Strait to the Holocene Thermal Maximum (12–5 kya), or a still more recent arrival or continued genetic exchange. We further assess the structure of the “invading” C. pallasii among and within the NE European seas, and document striking regional differences that contrast with the homogeneity of the herring stocks in their native basins. The data have implications on concepts of the systematics, breeding stocks and comparative genetics of C. pallasii itself, but are also of more general importance in the (comparative) framework of the history of boreal marine taxa with similar trans-Arctic distributions.
The dating of phylogeographical events on molecular grounds is a topic of contention due to the apparent time dependency of substitution rates (e.g. [23–25]), an issue that was also raised in previous herring work . We assess further the implications of the time dependency for the clupeid history and for inferences of trans-Arctic phylogeography more generally, by employing two sequence fragments of the mtDNA with potentially different mutation dynamics and biases (coding and non-coding).